Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes

Root-knot nematodes (RKN) are severe pests of maize. Although lipoxygenase (LOX) pathways and their oxylipin products have been implicated in plant–nematode interactions, prior to this report there was no conclusive genetic evidence for the function of any plant LOX gene in such interactions. We sho...

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Main Authors: Xiquan Gao, James Starr, Cornelia Göbel, Jürgen Engelberth, Ivo Feussner, James Tumlinson, Michael Kolomiets
Format: Article
Language:English
Published: The American Phytopathological Society 2008-01-01
Series:Molecular Plant-Microbe Interactions
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-1-0098
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author Xiquan Gao
James Starr
Cornelia Göbel
Jürgen Engelberth
Ivo Feussner
James Tumlinson
Michael Kolomiets
author_facet Xiquan Gao
James Starr
Cornelia Göbel
Jürgen Engelberth
Ivo Feussner
James Tumlinson
Michael Kolomiets
author_sort Xiquan Gao
collection DOAJ
description Root-knot nematodes (RKN) are severe pests of maize. Although lipoxygenase (LOX) pathways and their oxylipin products have been implicated in plant–nematode interactions, prior to this report there was no conclusive genetic evidence for the function of any plant LOX gene in such interactions. We showed that expression of a maize 9-LOX gene, ZmLOX3, increased steadily and peaked at 7 days after inoculation with Meloidogyne incognita RKN. Mu-insertional lox3-4 mutants displayed increased attractiveness to RKN and an increased number of juveniles and eggs. A set of jasmonic acid (JA)- and ethylene (ET)-responsive and biosynthetic genes as well as salicylic acid (SA)-dependent genes were overexpressed specifically in the roots of lox3-4 mutants. Consistent with this, levels of JA, SA, and ET were elevated in lox3-4 mutant roots, but not in leaves. Unlike wild types, in lox3-4 mutant roots, a phenylalanine ammonia lyase (PAL) gene was not RKN-inducible, suggesting a role for PAL-mediated metabolism in nematode resistance. In addition to these alterations in the defense status of roots, lox3-4 knockout mutants displayed precocious senescence and reduced root length and plant height compared with the wild type, suggesting that ZmLOX3 is required for normal plant development. Taken together, our data indicate that the ZmLOX3-mediated pathway may act as a root-specific suppressor of all three major defense signaling pathways to channel plant energy into growth processes, but is required for normal levels of resistance against nematodes.
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spelling doaj.art-8785bd06917347339c1bb5f45d34d6642022-12-22T03:04:55ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062008-01-012119810910.1094/MPMI-21-1-0098Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot NematodesXiquan GaoJames StarrCornelia GöbelJürgen EngelberthIvo FeussnerJames TumlinsonMichael KolomietsRoot-knot nematodes (RKN) are severe pests of maize. Although lipoxygenase (LOX) pathways and their oxylipin products have been implicated in plant–nematode interactions, prior to this report there was no conclusive genetic evidence for the function of any plant LOX gene in such interactions. We showed that expression of a maize 9-LOX gene, ZmLOX3, increased steadily and peaked at 7 days after inoculation with Meloidogyne incognita RKN. Mu-insertional lox3-4 mutants displayed increased attractiveness to RKN and an increased number of juveniles and eggs. A set of jasmonic acid (JA)- and ethylene (ET)-responsive and biosynthetic genes as well as salicylic acid (SA)-dependent genes were overexpressed specifically in the roots of lox3-4 mutants. Consistent with this, levels of JA, SA, and ET were elevated in lox3-4 mutant roots, but not in leaves. Unlike wild types, in lox3-4 mutant roots, a phenylalanine ammonia lyase (PAL) gene was not RKN-inducible, suggesting a role for PAL-mediated metabolism in nematode resistance. In addition to these alterations in the defense status of roots, lox3-4 knockout mutants displayed precocious senescence and reduced root length and plant height compared with the wild type, suggesting that ZmLOX3 is required for normal plant development. Taken together, our data indicate that the ZmLOX3-mediated pathway may act as a root-specific suppressor of all three major defense signaling pathways to channel plant energy into growth processes, but is required for normal levels of resistance against nematodes.https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-1-009812-oxo-phytodienoic acidfatty acid metabolismroot growth
spellingShingle Xiquan Gao
James Starr
Cornelia Göbel
Jürgen Engelberth
Ivo Feussner
James Tumlinson
Michael Kolomiets
Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
Molecular Plant-Microbe Interactions
12-oxo-phytodienoic acid
fatty acid metabolism
root growth
title Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
title_full Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
title_fullStr Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
title_full_unstemmed Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
title_short Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes
title_sort maize 9 lipoxygenase zmlox3 controls development root specific expression of defense genes and resistance to root knot nematodes
topic 12-oxo-phytodienoic acid
fatty acid metabolism
root growth
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-1-0098
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