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Article ; Online: Duplicated Copy Number Variant of the Maize 9-Lipoxygenase

Yuan, Peiguo / Huang, Pei-Cheng / Martin, Timothy K / Chappell, Thomas M / Kolomiets, Michael V

2024 Volume 15, Issue 4

Abstract: Extensive genome structure variations, such as copy number variations (CNVs) and presence/absence variations, are the basis for the remarkable genetic diversity of maize; however, the effect of CNVs on maize herbivory defense remains largely ... ...

Abstract	Extensive genome structure variations, such as copy number variations (CNVs) and presence/absence variations, are the basis for the remarkable genetic diversity of maize; however, the effect of CNVs on maize herbivory defense remains largely underexplored. Here, we report that the naturally occurring duplication of the maize 9-lipoxygenase gene
MeSH term(s)	Zea mays/genetics ; Zea mays/parasitology ; Animals ; DNA Copy Number Variations ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Lipoxygenase/genetics ; Herbivory ; Oxylipins/metabolism ; Plant Diseases/parasitology ; Plant Diseases/genetics
Chemical Substances	Plant Proteins ; Lipoxygenase (EC 1.13.11.12) ; Oxylipins
Language	English
Publishing date	2024-03-25
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes15040401
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Article ; Online: A non-JA producing oxophytodienoate reductase functions in salicylic acid-mediated antagonism with jasmonic acid during pathogen attack.

Huang, Pei-Cheng / Tate, Morgan / Berg-Falloure, Katherine M / Christensen, Shawn A / Zhang, Jinglan / Schirawski, Jan / Meeley, Robert / Kolomiets, Michael V

Molecular plant pathology

2023 Volume 24, Issue 7, Page(s) 725–741

Abstract: Peroxisome-localized oxo-phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12-OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non-JA producing OPRs remain largely unknown. Here, we ... ...

Abstract	Peroxisome-localized oxo-phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12-OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non-JA producing OPRs remain largely unknown. Here, we generated Mutator-insertional mutants of the maize OPR2 gene and tested its role in resistance to pathogens with distinct lifestyles. Functional analyses showed that the opr2 mutants were more susceptible to the (hemi)biotrophic pathogens Colletotrichum graminicola and Ustilago maydis, but were more resistant to the necrotrophic fungus Cochliobolus heterostrophus. Hormone profiling revealed that increased susceptibility to C. graminicola was associated with decreased salicylic acid (SA) but increased JA levels. Mutation of the JA-producing lipoxygenase 10 (LOX10) reversed this phenotype in the opr2 mutant background, corroborating the notion that JA promotes susceptibility to this pathogen. Exogenous SA did not rescue normal resistance levels in opr2 mutants, suggesting that this SA-inducible gene is the key downstream component of the SA-mediated defences against C. graminicola. Disease assays of the single and double opr2 and lox10 mutants and the JA-deficient opr7opr8 mutants showed that OPR2 negatively regulates JA biosynthesis, and that JA is required for resistance against C. heterostrophus. Overall, this study uncovers a novel function of a non-JA producing OPR as a major negative regulator of JA biosynthesis during pathogen infection, a function that leads to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle.
MeSH term(s)	Oxidoreductases ; Salicylic Acid ; Oxylipins ; Cyclopentanes ; Gene Expression Regulation, Plant
Chemical Substances	jasmonic acid (6RI5N05OWW) ; Oxidoreductases (EC 1.-) ; Salicylic Acid (O414PZ4LPZ) ; 2-(2'-pyridyldithio)benzyldiazoacetate (63681-84-5) ; Oxylipins ; Cyclopentanes
Language	English
Publishing date	2023-01-30
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1364-3703
ISSN (online)	1364-3703
ISSN	1364-3703
DOI	10.1111/mpp.13299
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Article ; Online: Maize OPR2 and LOX10 Mediate Defense against Fall Armyworm and Western Corn Rootworm by Tissue-Specific Regulation of Jasmonic Acid and Ketol Metabolism.

Huang, Pei-Cheng / Grunseich, John M / Berg-Falloure, Katherine M / Tolley, Jordan P / Koiwa, Hisashi / Bernal, Julio S / Kolomiets, Michael V

Genes

2023 Volume 14, Issue 9

Abstract: Foliage-feeding fall armyworm (FAW; ...

Abstract	Foliage-feeding fall armyworm (FAW;
Language	English
Publishing date	2023-08-30
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes14091732
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Article ; Online: A non‐JA producing oxophytodienoate reductase functions in salicylic acid‐mediated antagonism with jasmonic acid during pathogen attack

Huang, Pei‐Cheng / Tate, Morgan / Berg‐Falloure, Katherine M. / Christensen, Shawn A. / Zhang, Jinglan / Schirawski, Jan / Meeley, Robert / Kolomiets, Michael V.

Molecular Plant Pathology. 2023 July, v. 24, no. 7 p.725-741

2023

Abstract: Peroxisome‐localized oxo‐phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12‐OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non‐JA producing OPRs remain largely unknown. Here, we ... ...

Abstract	Peroxisome‐localized oxo‐phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12‐OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non‐JA producing OPRs remain largely unknown. Here, we generated Mutator‐insertional mutants of the maize OPR2 gene and tested its role in resistance to pathogens with distinct lifestyles. Functional analyses showed that the opr2 mutants were more susceptible to the (hemi)biotrophic pathogens Colletotrichum graminicola and Ustilago maydis, but were more resistant to the necrotrophic fungus Cochliobolus heterostrophus. Hormone profiling revealed that increased susceptibility to C. graminicola was associated with decreased salicylic acid (SA) but increased JA levels. Mutation of the JA‐producing lipoxygenase 10 (LOX10) reversed this phenotype in the opr2 mutant background, corroborating the notion that JA promotes susceptibility to this pathogen. Exogenous SA did not rescue normal resistance levels in opr2 mutants, suggesting that this SA‐inducible gene is the key downstream component of the SA‐mediated defences against C. graminicola. Disease assays of the single and double opr2 and lox10 mutants and the JA‐deficient opr7opr8 mutants showed that OPR2 negatively regulates JA biosynthesis, and that JA is required for resistance against C. heterostrophus. Overall, this study uncovers a novel function of a non‐JA producing OPR as a major negative regulator of JA biosynthesis during pathogen infection, a function that leads to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle.
Keywords	Bipolaris maydis ; Glomerella graminicola ; Ustilago zeae ; antagonism ; biosynthesis ; corn ; fungi ; genes ; jasmonic acid ; lifestyle ; lipoxygenases ; mutants ; mutation ; pathogens ; phenotype ; plant pathology ; salicylic acid
Language	English
Dates of publication	2023-07
Size	p. 725-741.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1464-6722
ISSN (online)	1364-3703
ISSN	1464-6722
DOI	10.1111/mpp.13299
Database	NAL-Catalogue (AGRICOLA)

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Article: Trichoderma virens

Huang, Pei-Cheng / Yuan, Peiguo / Grunseich, John M / Taylor, James / Tiénébo, Eric-Olivier / Pierson, Elizabeth A / Bernal, Julio S / Kenerley, Charles M / Kolomiets, Michael V

Plants (Basel, Switzerland)

2024 Volume 13, Issue 9

Abstract: ... Soil- ... ...

Abstract	Soil-borne
Language	English
Publishing date	2024-04-30
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2704341-1
ISSN	2223-7747
ISSN	2223-7747
DOI	10.3390/plants13091240
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Article: Raman Spectroscopy as a Robust New Tool for Rapid and Accurate Evaluation of Drought Tolerance Levels in Both Genetically Diverse and Near-Isogenic Maize Lines.

Altangerel, Narangerel / Huang, Pei-Cheng / Kolomiets, Michael V / Scully, Marlan O / Hemmer, Philip R

Frontiers in plant science

2021 Volume 12, Page(s) 621711

Abstract: Improving drought tolerance of crops has become crucial due to the current scenario of rapid climate change. In particular, development of new maize germplasm with increased drought tolerance is viewed as a major breeding goal to ensure sustainable food ... ...

Abstract	Improving drought tolerance of crops has become crucial due to the current scenario of rapid climate change. In particular, development of new maize germplasm with increased drought tolerance is viewed as a major breeding goal to ensure sustainable food and feed production. Therefore, accurate rapid phenotyping techniques for selection of superior maize genotypes are required. The objectives of this study were to determine whether Raman microscopy technique can be applied for accurate assessment of drought-tolerance levels in both genetically diverse and near-isogenic maize lines that differ in their levels of drought-tolerance. Carotenoid degradation is known to be a direct stress response initiated by reactive oxygen species during osmotic stress such as drought. Using Raman mapping, we observed real-time changes in the rate of carotenoid degradation in chloroplasts that was dependent on the strength of osmotic stress. In addition, we showed that the rate of carotenoid degradation as measured by Raman spectroscopy correlates directly with drought tolerance levels of diverse maize genotypes. We conclude that Raman technique is a robust, biochemically selective and non-invasive phenotyping technique that accurately distinguishes drought tolerance levels in both genetically diverse and near-isogenic maize genotypes. We conclude that this technique can be further developed to render it suitable for field-based early assessment of breeding materials with superior drought-tolerance traits.
Language	English
Publishing date	2021-07-12
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2021.621711
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Article: Trichoderma virens colonization of maize roots triggers rapid accumulation of 12-oxophytodienoate and two ᵧ-ketols in leaves as priming agents of induced systemic resistance

Wang, Ken-Der / Gorman, Zachary / Huang, Pei-Cheng / Kenerley, Charles M / Kolomiets, Michael V

Plant signaling & behavior. 2020 Sept. 01, v. 15, no. 9

2020

Abstract: Two oxylipins 12-OPDA (12-Oxo-10(Z),15(Z)-phytodienoic acid) and an ᵧ-ketol, 9,10-KODA (10-oxo-9-hydroxy-12(Z), 15(Z)-octadecadienoic acid) were recently identified as important long-distance-induced systemic resistance (ISR) signals in Trichoderma ... ...

Abstract	Two oxylipins 12-OPDA (12-Oxo-10(Z),15(Z)-phytodienoic acid) and an ᵧ-ketol, 9,10-KODA (10-oxo-9-hydroxy-12(Z), 15(Z)-octadecadienoic acid) were recently identified as important long-distance-induced systemic resistance (ISR) signals in Trichoderma virens-treated maize. On the other hand, jasmonic acid (JA), long believed to be a major signal of ISR, was not involved, as the JA-deficient mutant, opr7 opr8, retained the capacity for T. virens-triggered ISR. In order to further understand the biochemical basis for ISR priming in maize leaves, diverse oxylipins and phytohormones in the leaves of wild-type maize or ISR-deficient lox10-3 mutants treated with T. virens were quantified. This analysis revealed that 12-OPDA and two novel ᵧ-ketols, 9,12-KOMA (12-Oxo-9-hydroxy-10(E)-octadecenoic acid) and 9,12-KODA (12-Oxo-9-hydroxy-10(E),15(Z)-octadecadienoic acid), accumulated at high levels in ISR-positive plants. In support of the notion that 12-OPDA serves as a priming agent for ISR in addition to being a xylem-mobile signal, leaf pretreatment with this JA precursor resulted in increased resistance to Colletotrichum graminicola. Furthermore, the injection of 9,12-KODA or 9,12-KOMA in wild-type plants enhanced resistance against C. graminicola infection, suggesting that they play roles in ISR priming.
Keywords	Glomerella graminicola ; Trichoderma virens ; behavior ; corn ; jasmonic acid ; leaves ; mutants ; oxylipins ; plant hormones ; systemic acquired resistance
Language	English
Dates of publication	2020-0901
Publishing place	Taylor & Francis
Document type	Article
Note	NAL-AP-2-clean
ISSN	1559-2324
DOI	10.1080/15592324.2020.1792187
Database	NAL-Catalogue (AGRICOLA)

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Article: Relative contribution of LOX10, green leaf volatiles and JA to wound-induced local and systemic oxylipin and hormone signature in Zea mays (maize)

He, Yongming / Borrego, Eli J / Gorman, Zachary / Huang, Pei-Cheng / Kolomiets, Michael V

Phytochemistry. 2020 June, v. 174

2020

Abstract: Green leaf volatiles (GLVs) and jasmonates (JAs) are the best-characterized groups of fatty acid-derived oxylipin signals that regulate wound-associated defenses. Beyond these two major groups of defense signals, plants produce an array of oxylipins in ... ...

Abstract	Green leaf volatiles (GLVs) and jasmonates (JAs) are the best-characterized groups of fatty acid-derived oxylipin signals that regulate wound-associated defenses. Beyond these two major groups of defense signals, plants produce an array of oxylipins in response to wounding, which possess potent signaling and/or insecticidal activities. In this study, we assessed the relative contribution of JAs and GLVs to wound-induced systemic signaling and the associated regulation of oxylipins in local and systemic tissues of maize (Zea mays). For this, we utilized GLV- and JA-deficient mutants, lox10 single and opr7opr8 double mutants, respectively, and profiled oxylipins in untreated leaves and roots, and in locally wounded and systemic leaves. In contrast to the studies in dicots, no systemic induction of JAs was observed in maize. Instead, a JA precursor, 12-OPDA, as well as ketols and C12/13 oxo-acids derived from 13-lipoxygenases (LOXs), were preferentially induced in both locally wounded and systemic unwounded leaves. Several 9-LOX-derived oxylipins (9-oxylipins) including hydroxides and ketones were also significantly induced locally. JA and JA-isoleucine (JA-Ile) were rapidly induced within 0.5 h, and were followed by a second increase in local tissue 4 h after wounding. GLV-deficient lox10 mutants displayed reduced levels of most 13-oxylipins, and elevated levels of several 9-oxylipins and the a-dioxygenase (DOX) product, 2-HOD. lox10 mutants were completely devoid of C6 volatiles and their C12 counterparts, and greatly decreased in C5 volatiles and their C13 oxo-acid counterparts. Thus, in addition to being the sole LOX isoform providing substrate for GLV synthesis, LOX10 is a major 13-LOX that provides substrate to several LOX branches that produce an array of 13-oxylipin products, including C5 volatiles. Interestingly, the rapid JA and JA-Ile increase at 0.5–2 h post-wounding was only moderately affected by the LOX10 mutation, while significantly reduced levels were observed at 4 h post-wounding. Combined with the previous findings that GLVs activate JA biosynthesis, these results suggest that both LOX10-derived substrates and/or GLVs are involved in the large second phase of JA synthesis proximal to the wound. Analyses of opr7opr8 mutants revealed that wound-induced oxylipin responses were positively regulated by JA signaling. The local and systemic accumulation of SA was not altered in the two mutants. Collectively, our results identified a subset of oxylipins strongly induced in wounded and systemic leaves, but their impact on insect defenses remain elusive. The lack of systemic induction of JAs points to substantial difference between systemic wound responses in studied dicots and maize. Our results show that GLV-deficiency and reduced JA in lox10 mutants had a greater impact on wound-induced local and systemic tissue oxylipin responses compared to the solely JA-deficient opr7opr8 double mutants. This suggests that GLVs or other LOX10-derived products heavily contribute to overall basal and wound-induced oxylipin responses. The specific roles of the GLV- and/or JA-dependent oxylipins in wound responses and defense remain to be further investigated by a combination of multiple orders of oxylipin-deficient mutants.
Keywords	Magnoliopsida ; Zea mays ; biosynthesis ; corn ; enzymes ; hydroxides ; insecticidal properties ; jasmonic acid ; keto acids ; leaves ; mutants ; mutation ; oxylipins ; roots ; tissues
Language	English
Dates of publication	2020-06
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	208884-8
ISSN	1873-3700 ; 0031-9422
ISSN (online)	1873-3700
ISSN	0031-9422
DOI	10.1016/j.phytochem.2020.112334
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: 9,10-KODA, an α-ketol produced by the tonoplast-localized 9-lipoxygenase ZmLOX5, plays a signaling role in maize defense against insect herbivory

Yuan, Peiguo / Borrego, Eli / Park, Yong-Soon / Gorman, Zachary / Huang, Pei-Cheng / Tolley, Jordan / Christensen, Shawn A. / Blanford, Jantana / Kilaru, Aruna / Meeley, Robert / Koiwa, Hisashi / Vidal, Stefan / Huffaker, Alisa / Schmelz, Eric / Kolomiets, Michael V.

Molecular Plant. 2023 July 11,

2023

Abstract: 13-Lipoxygenases (LOXs) initiate the synthesis of jasmonic acid (JA), the best-understood oxylipin hormone in herbivory defense. However, the roles of 9-LOX-derived oxylipins in insect resistance remain unclear. Here, we report a novel anti-herbivory ... ...

Abstract	13-Lipoxygenases (LOXs) initiate the synthesis of jasmonic acid (JA), the best-understood oxylipin hormone in herbivory defense. However, the roles of 9-LOX-derived oxylipins in insect resistance remain unclear. Here, we report a novel anti-herbivory mechanism mediated by a tonoplast-localized 9-LOX, ZmLOX5, and its linolenic acid-derived product, 9-hydroxy-10-oxo-12(Z),15(Z)-octadecadienoic acid (9,10-KODA). Transposon-insertional disruption of ZmLOX5 resulted in the loss of resistance to insect herbivory. lox5 knockout mutants displayed greatly reduced wound-induced accumulation of multiple oxylipins and defense metabolites, including benzoxazinoids, abscisic acid (ABA), and JA-isoleucine (JA-Ile). However, exogenous JA-Ile failed to rescue insect defense in lox5 mutants, while applications of 1 μM 9,10-KODA or the JA precursor, 12-oxo-phytodienoic acid (12-OPDA), restored wild-type resistance levels. Metabolite profiling revealed that exogenous 9,10-KODA primed the plants for increased production of ABA and 12-OPDA, but not JA-Ile. While none of the 9-oxylipins were able to rescue JA-Ile induction, the lox5 mutant accumulated lower wound-induced levels of Ca²⁺, suggesting this as a potential explanation for lower wound-induced JA. Seedlings pretreated with 9,10-KODA exhibited rapid or more robust wound-induced defense gene expression. In addition, an artificial diet supplemented with 9,10-KODA arrested fall armyworm larvae growth. Finally, analysis of single and double lox5 and lox10 mutants showed that ZmLOX5 also contributed to insect defense by modulating ZmLOX10-mediated green leaf volatile signaling. Collectively, our study uncovered a previously unknown anti-herbivore defense and hormone-like signaling activity for a major 9-oxylipin α-ketol.
Keywords	Spodoptera frugiperda ; abscisic acid ; artificial diets ; benzoxazinoids ; calcium ; corn ; gene expression ; herbivores ; insect resistance ; insects ; jasmonic acid ; leaves ; metabolites ; mutants ; oxylipins ; defense priming ; fall armyworm ; Spodoptera ; 12-oxo-phytodienoic acid ; vacuole
Language	English
Dates of publication	2023-0711
Publishing place	Elsevier Inc.
Document type	Article ; Online
Note	Pre-press version
ZDB-ID	2393618-6
ISSN	1752-9867 ; 1674-2052
ISSN (online)	1752-9867
ISSN	1674-2052
DOI	10.1016/j.molp.2023.07.003
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Article ; Online: Trichoderma virens

Wang, Ken-Der / Gorman, Zachary / Huang, Pei-Cheng / Kenerley, Charles M / Kolomiets, Michael V

Plant signaling & behavior

2020 Volume 15, Issue 9, Page(s) 1792187

Abstract: Two oxylipins 12-OPDA (12-Oxo-10( ...

Abstract	Two oxylipins 12-OPDA (12-Oxo-10(
MeSH term(s)	Colletotrichum/pathogenicity ; Disease Resistance ; Fatty Acids, Unsaturated/metabolism ; Oxylipins/metabolism ; Plant Leaves/metabolism ; Plant Leaves/microbiology ; Zea mays/metabolism ; Zea mays/microbiology
Chemical Substances	Fatty Acids, Unsaturated ; Oxylipins ; 12-oxophytodienoic acid (67204-66-4)
Language	English
Publishing date	2020-07-11
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1559-2324
ISSN (online)	1559-2324
DOI	10.1080/15592324.2020.1792187
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