NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth

Qiujie Liu; Mary Galli; Xue Liu; Silvia Federici; Amy Buck; Jon Cody; Massimo Labra; Andrea Gallavotti

doi:10.1073/pnas.1907071116

NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth

Qiujie Liu, Mary Galli, Xue Liu, Silvia Federici, Amy Buck, Jon Cody, Massimo Labra, Andrea Gallavotti

Genetics, Cell Biology and Development (CBS)

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

29 Scopus citations

Abstract

Meristems are highly regulated structures ultimately responsible for the formation of branches, lateral organs, and stems, and thus directly affect plant architecture and crop yield. In meristems, genetic networks, hormones, and signaling molecules are tightly integrated to establish robust systems that can adapt growth to continuous inputs from the environment. Here we characterized needle1 (ndl1), a temperature-sensitive maize mutant that displays severe reproductive defects and strong genetic interactions with known mutants affected in the regulation of the plant hormone auxin. NDL1 encodes amitochondria-localized ATP-dependent metalloprotease belonging to the FILAMENTATION TEMPERATURESENSITIVE H (FTSH) family. Together with the hyperaccumulation of reactive oxygen species (ROS), ndl1 inflorescences show upregulation of a plethora of stress-response genes. We provide evidence that these conditions alter endogenous auxin levels and disrupt primordia initiation in meristems. These findings connect meristem redox status and auxin in the control of maize growth.

Original language	English (US)
Pages (from-to)	19736-19742
Number of pages	7
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	39
DOIs	https://doi.org/10.1073/pnas.1907071116
State	Published - Sep 24 2019

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. The authors thank Dr. Gerald Neuffer for generating the ndl1-ref allele, the Maize Genetics Cooperation Stock Center for seeds, Renyta Moses and Gabriel Koslow for help with genotyping, Paula McSteen and the University of Missouri Columbia Plant Transformation Core Facility for transformation, Robert Schmitz and the Georgia University Genetic Department for RNA-seq sequencing, Yaping Feng for assistance with BSA RNA-seq, and Carolyn Rasmussen for DII-VENUS seeds and comments on the manuscript. Q.L. was supported by the China Scholarship Council and by the Waksman Charles and Johanna Busch Fellowship. This research was supported by grants from the National Science Foundation (IOS 1546873 and 1456950 to A.G.).

Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.

Keywords

Auxin
FTSH
Maize
Meristems
ROS

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10.1073/pnas.1907071116

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title = "NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth",

abstract = "Meristems are highly regulated structures ultimately responsible for the formation of branches, lateral organs, and stems, and thus directly affect plant architecture and crop yield. In meristems, genetic networks, hormones, and signaling molecules are tightly integrated to establish robust systems that can adapt growth to continuous inputs from the environment. Here we characterized needle1 (ndl1), a temperature-sensitive maize mutant that displays severe reproductive defects and strong genetic interactions with known mutants affected in the regulation of the plant hormone auxin. NDL1 encodes amitochondria-localized ATP-dependent metalloprotease belonging to the FILAMENTATION TEMPERATURESENSITIVE H (FTSH) family. Together with the hyperaccumulation of reactive oxygen species (ROS), ndl1 inflorescences show upregulation of a plethora of stress-response genes. We provide evidence that these conditions alter endogenous auxin levels and disrupt primordia initiation in meristems. These findings connect meristem redox status and auxin in the control of maize growth.",

keywords = "Auxin, FTSH, Maize, Meristems, ROS",

author = "Qiujie Liu and Mary Galli and Xue Liu and Silvia Federici and Amy Buck and Jon Cody and Massimo Labra and Andrea Gallavotti",

note = "Funding Information: ACKNOWLEDGMENTS. The authors thank Dr. Gerald Neuffer for generating the ndl1-ref allele, the Maize Genetics Cooperation Stock Center for seeds, Renyta Moses and Gabriel Koslow for help with genotyping, Paula McSteen and the University of Missouri Columbia Plant Transformation Core Facility for transformation, Robert Schmitz and the Georgia University Genetic Department for RNA-seq sequencing, Yaping Feng for assistance with BSA RNA-seq, and Carolyn Rasmussen for DII-VENUS seeds and comments on the manuscript. Q.L. was supported by the China Scholarship Council and by the Waksman Charles and Johanna Busch Fellowship. This research was supported by grants from the National Science Foundation (IOS 1546873 and 1456950 to A.G.). Publisher Copyright: {\textcopyright} 2019 National Academy of Sciences. All rights reserved.",

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AU - Galli, Mary

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AU - Federici, Silvia

AU - Buck, Amy

AU - Cody, Jon

AU - Labra, Massimo

AU - Gallavotti, Andrea

N1 - Funding Information: ACKNOWLEDGMENTS. The authors thank Dr. Gerald Neuffer for generating the ndl1-ref allele, the Maize Genetics Cooperation Stock Center for seeds, Renyta Moses and Gabriel Koslow for help with genotyping, Paula McSteen and the University of Missouri Columbia Plant Transformation Core Facility for transformation, Robert Schmitz and the Georgia University Genetic Department for RNA-seq sequencing, Yaping Feng for assistance with BSA RNA-seq, and Carolyn Rasmussen for DII-VENUS seeds and comments on the manuscript. Q.L. was supported by the China Scholarship Council and by the Waksman Charles and Johanna Busch Fellowship. This research was supported by grants from the National Science Foundation (IOS 1546873 and 1456950 to A.G.). Publisher Copyright: © 2019 National Academy of Sciences. All rights reserved.

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N2 - Meristems are highly regulated structures ultimately responsible for the formation of branches, lateral organs, and stems, and thus directly affect plant architecture and crop yield. In meristems, genetic networks, hormones, and signaling molecules are tightly integrated to establish robust systems that can adapt growth to continuous inputs from the environment. Here we characterized needle1 (ndl1), a temperature-sensitive maize mutant that displays severe reproductive defects and strong genetic interactions with known mutants affected in the regulation of the plant hormone auxin. NDL1 encodes amitochondria-localized ATP-dependent metalloprotease belonging to the FILAMENTATION TEMPERATURESENSITIVE H (FTSH) family. Together with the hyperaccumulation of reactive oxygen species (ROS), ndl1 inflorescences show upregulation of a plethora of stress-response genes. We provide evidence that these conditions alter endogenous auxin levels and disrupt primordia initiation in meristems. These findings connect meristem redox status and auxin in the control of maize growth.

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NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth

Abstract

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