Publications by authors named "Eric A Schmelz"

77 Publications

Getting back to the grass roots: harnessing specialized metabolites for improved crop stress resilience.

Curr Opin Biotechnol 2021 Aug 12;70:174-186. Epub 2021 Jun 12.

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, USA. Electronic address:

Roots remain an understudied site of complex and important biological interactions mediating plant productivity. In grain and bioenergy crops, grass root specialized metabolites (GRSM) are central to key interactions, yet our basic knowledge of the chemical language remains fragmentary. Continued improvements in plant genome assembly and metabolomics are enabling large-scale advances in the discovery of specialized metabolic pathways as a means of regulating root-biotic interactions. Metabolomics, transcript coexpression analyses, forward genetic studies, gene synthesis and heterologous expression assays drive efficient pathway discoveries. Functional genetic variants identified through genome wide analyses, targeted CRISPR/Cas9 approaches, and both native and non-native overexpression studies critically inform novel strategies for bioengineering metabolic pathways to improve plant traits.
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http://dx.doi.org/10.1016/j.copbio.2021.05.010DOI Listing
August 2021

Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against and Its Satellites.

mBio 2021 02 16;12(1). Epub 2021 Feb 16.

Texas A&M AgriLife Research and Extension Center, Texas A&M University System, Weslaco, Texas, USA

has recently emerged as a premier model plant for monocot biology, akin to We previously reported genome-wide transcriptomic and alternative splicing changes occurring in during compatible infections with (PMV) and its satellite virus (SPMV). Here, we dissected the role of phenylalanine ammonia lyase 1 (PAL1), a key enzyme for phenylpropanoid and salicylic acid (SA) biosynthesis and the induction of plant defenses. Targeted metabolomics profiling of PMV-infected and PMV- plus SPMV-infected (PMV/SPMV) plants revealed enhanced levels of multiple defense-related hormones and metabolites such as cinnamic acid, SA, and fatty acids and lignin precursors during disease progression. The virus-induced accumulation of SA and lignin was significantly suppressed upon knockdown of () using RNA interference (RNAi). The compromised SA accumulation in PMV/SPMV-infected RNAi plants correlated with weaker induction of multiple SA-related defense gene markers (pathogenesis related 1 [], , , and ) and enhanced susceptibility to PMV/SPMV compared to that of wild-type (WT) plants. Furthermore, exogenous application of SA alleviated the PMV/SPMV necrotic disease phenotypes and delayed plant death caused by single and mixed infections. Together, our results support an antiviral role for during compatible host-virus interaction, perhaps as a last resort attempt to rescue the infected plant. Although the role of plant defense mechanisms against viruses are relatively well studied in dicots and in incompatible plant-microbe interactions, studies of their roles in compatible interactions and in grasses are lagging behind. In this study, we leveraged the emerging grass model and genetic resources to dissect (PMV)- and its satellite virus (SPMV)-compatible grass-virus interactions. We found a significant role for PAL1 in the production of salicylic acid (SA) in response to PMV/SPMV infections and that SA is an essential component of the defense response preventing the plant from succumbing to viral infection. Our results suggest a convergent role for the SA defense pathway in both compatible and incompatible plant-virus interactions and underscore the utility of for grass-virus biology.
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http://dx.doi.org/10.1128/mBio.03518-20DOI Listing
February 2021

A receptor-like protein mediates plant immune responses to herbivore-associated molecular patterns.

Proc Natl Acad Sci U S A 2020 12 23;117(49):31510-31518. Epub 2020 Nov 23.

Section of Cell and Developmental Biology, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093;

Herbivory is fundamental to the regulation of both global food webs and the extent of agricultural crop losses. Induced plant responses to herbivores promote resistance and often involve the perception of specific herbivore-associated molecular patterns (HAMPs); however, precisely defined receptors and elicitors associated with herbivore recognition remain elusive. Here, we show that a receptor confers signaling and defense outputs in response to a defined HAMP common in caterpillar oral secretions (OS). Staple food crops, including cowpea () and common bean (), specifically respond to OS via recognition of proteolytic fragments of chloroplastic ATP synthase, termed inceptins. Using forward-genetic mapping of inceptin-induced plant responses, we identified a corresponding leucine-rich repeat receptor, termed INR, specific to select legume species and sufficient to confer inceptin-induced responses and enhanced defense against armyworms () in tobacco. Our results support the role of plant immune receptors in the perception of chewing herbivores and defense.
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http://dx.doi.org/10.1073/pnas.2018415117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7733821PMC
December 2020

Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity.

Nat Plants 2020 11 26;6(11):1375-1388. Epub 2020 Oct 26.

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, USA.

Specialized metabolites constitute key layers of immunity that underlie disease resistance in crops; however, challenges in resolving pathways limit our understanding of the functions and applications of these metabolites. In maize (Zea mays), the inducible accumulation of acidic terpenoids is increasingly considered to be a defence mechanism that contributes to disease resistance. Here, to understand maize antibiotic biosynthesis, we integrated association mapping, pan-genome multi-omic correlations, enzyme structure-function studies and targeted mutagenesis. We define ten genes in three zealexin (Zx) gene clusters that encode four sesquiterpene synthases and six cytochrome P450 proteins that collectively drive the production of diverse antibiotic cocktails. Quadruple mutants in which the ability to produce zealexins (ZXs) is blocked exhibit a broad-spectrum loss of disease resistance. Genetic redundancies ensuring pathway resiliency to single null mutations are combined with enzyme substrate promiscuity, creating a biosynthetic hourglass pathway that uses diverse substrates and in vivo combinatorial chemistry to yield complex antibiotic blends. The elucidated genetic basis of biochemical phenotypes that underlie disease resistance demonstrates a predominant maize defence pathway and informs innovative strategies for transferring chemical immunity between crops.
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http://dx.doi.org/10.1038/s41477-020-00787-9DOI Listing
November 2020

Survey of Sensitivity to Fatty Acid-Amino Acid Conjugates in the Solanaceae.

J Chem Ecol 2020 Mar 27;46(3):330-343. Epub 2020 Jan 27.

Department of Biological Sciences, University of South Carolina, Columbia, SC, USA.

Plants perceive insect herbivores via a sophisticated surveillance system that detects a range of alarm signals, including herbivore-associated molecular patterns (HAMPs). Fatty acid-amino acid conjugates (FACs) are HAMPs present in oral secretions (OS) of lepidopteran larvae that induce defense responses in many plant species. In contrast to eggplant (Solanum melongena), tomato (S. lycopersicum) does not respond to FACs present in OS from Manduca sexta (Lepidoptera). Since both plants are found in the same genus, we tested whether loss of sensitivity to FACs in tomato may be a domestication effect. Using highly sensitive MAP kinase (MAPK) phosphorylation assays, we demonstrate that four wild tomato species and the closely related potato (S. tuberosum) do not respond to the FACs N-linolenoyl-L-glutamine and N-linolenoyl-L-glutamic acid, excluding a domestication effect. Among other genera within the Solanaceae, we found that bell pepper (Capsicum annuum) is responsive to FACs, while there is a differential responsiveness to FACs among tobacco (Nicotiana) species, ranging from strong responsiveness in N. benthamiana to no responsiveness in N. knightiana. The Petunia lineage is one of the oldest lineages within the Solanaceae and P. hybrida was responsive to FACs. Collectively, we demonstrate that plant responsiveness to FACs does not follow simple phylogenetic relationships in the family Solanaceae. Instead, sensitivity to FACs is a dynamic ancestral trait present in monocots and eudicots that was repeatedly lost during the evolution of Solanaceae species. Although tomato is insensitive to FACs, we found that other unidentified factors in M. sexta OS induce defenses in tomato.
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http://dx.doi.org/10.1007/s10886-020-01152-yDOI Listing
March 2020

Multiple genes recruited from hormone pathways partition maize diterpenoid defences.

Nat Plants 2019 10 16;5(10):1043-1056. Epub 2019 Sep 16.

Section of Cell and Developmental Biology, University of California San Diego, La Jolla, CA, USA.

Duplication and divergence of primary pathway genes underlie the evolution of plant specialized metabolism; however, mechanisms partitioning parallel hormone and defence pathways are often speculative. For example, the primary pathway intermediate ent-kaurene is essential for gibberellin biosynthesis and is also a proposed precursor for maize antibiotics. By integrating transcriptional coregulation patterns, genome-wide association studies, combinatorial enzyme assays, proteomics and targeted mutant analyses, we show that maize kauralexin biosynthesis proceeds via the positional isomer ent-isokaurene formed by a diterpene synthase pair recruited from gibberellin metabolism. The oxygenation and subsequent desaturation of ent-isokaurene by three promiscuous cytochrome P450s and a new steroid 5α reductase indirectly yields predominant ent-kaurene-associated antibiotics required for Fusarium stalk rot resistance. The divergence and differential expression of pathway branches derived from multiple duplicated hormone-metabolic genes minimizes dysregulation of primary metabolism via the circuitous biosynthesis of ent-kaurene-related antibiotics without the production of growth hormone precursors during defence.
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http://dx.doi.org/10.1038/s41477-019-0509-6DOI Listing
October 2019

Functional Characterization of Two Class II Diterpene Synthases Indicates Additional Specialized Diterpenoid Pathways in Maize ().

Front Plant Sci 2018 23;9:1542. Epub 2018 Oct 23.

Department of Plant Biology, University of California, Davis, Davis, CA, United States.

As a major staple food, maize () is critical to food security. Shifting environmental pressures increasingly hamper crop defense capacities, causing expanded harvest loss. Specialized labdane-type diterpenoids are key components of maize chemical defense and ecological adaptation. Labdane diterpenoid biosynthesis most commonly requires the pairwise activity of class II and class I diterpene synthases (diTPSs) that convert the central precursor geranylgeranyl diphosphate into distinct diterpenoid scaffolds. Two maize class II diTPSs, ANTHER EAR 1 and 2 (ZmAN1/2), have been previously identified as catalytically redundant -copalyl diphosphate (CPP) synthases. ZmAN1 is essential for gibberellin phytohormone biosynthesis, whereas ZmAN2 is stress-inducible and governs the formation of defensive kauralexin and dolabralexin diterpenoids. Here, we report the biochemical characterization of the two remaining class II diTPSs present in the maize genome, COPALYL DIPHOSPHATE SYNTHASE 3 (ZmCPS3) and COPALYL DIPHOSPHATE SYNTHASE 4 (ZmCPS4). Functional analysis via microbial co-expression assays identified ZmCPS3 as a (+)-CPP synthase, with functionally conserved orthologs occurring in wheat () and numerous dicot species. ZmCPS4 formed the unusual prenyl diphosphate, 8,13-CPP (labda-8,13-dien-15-yl diphosphate), as verified by mass spectrometry and nuclear magnetic resonance. As a minor product, ZmCPS4 also produced labda-13-en-8-ol diphosphate (LPP). Root gene expression profiles did not indicate an inducible role of in maize stress responses. By contrast, showed a pattern of inducible gene expression in roots exposed to oxidative stress, supporting a possible role in abiotic stress responses. Identification of the catalytic activities of ZmCPS3 and ZmCPS4 clarifies the first committed reactions controlling the diversity of defensive diterpenoids in maize, and suggests the existence of additional yet undiscovered diterpenoid pathways.
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http://dx.doi.org/10.3389/fpls.2018.01542DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206430PMC
October 2018

Ethylene signaling regulates natural variation in the abundance of antifungal acetylated diferuloylsucroses and Fusarium graminearum resistance in maize seedling roots.

New Phytol 2019 03 2;221(4):2096-2111. Epub 2018 Nov 2.

Boyce Thompson Institute, 533 Tower Road, Ithaca, NY, 14853, USA.

The production and regulation of defensive specialized metabolites play a central role in pathogen resistance in maize (Zea mays) and other plants. Therefore, identification of genes involved in plant specialized metabolism can contribute to improved disease resistance. We used comparative metabolomics to identify previously unknown antifungal metabolites in maize seedling roots, and investigated the genetic and physiological mechanisms underlying their natural variation using quantitative trait locus mapping and comparative transcriptomics approaches. Two maize metabolites, smilaside A (3,6-diferuloyl-3',6'-diacetylsucrose) and smiglaside C (3,6-diferuloyl-2',3',6'-triacetylsucrose), were identified that could contribute to maize resistance against Fusarium graminearum and other fungal pathogens. Elevated expression of an ethylene signaling gene, ETHYLENE INSENSITIVE 2 (ZmEIN2), co-segregated with a decreased smilaside A : smiglaside C ratio. Pharmacological and genetic manipulation of ethylene availability and sensitivity in vivo indicated that, whereas ethylene was required for the production of both metabolites, the smilaside A : smiglaside C ratio was negatively regulated by ethylene sensitivity. This ratio, rather than the absolute abundance of these two metabolites, was important for maize seedling root defense against F. graminearum. Ethylene signaling regulates the relative abundance of the two F. graminearum-resistance-related metabolites and affects resistance against F. graminearum in maize seedling roots.
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http://dx.doi.org/10.1111/nph.15520DOI Listing
March 2019

Biosynthesis and function of terpenoid defense compounds in maize (Zea mays).

Planta 2019 Jan 6;249(1):21-30. Epub 2018 Sep 6.

Center for Medical, Agricultural and Veterinary Entomology, U.S. Department of Agriculture-Agricultural Research Service, 1700 SW 23rd Drive, Gainesville, FL, 32608, USA.

Main Conclusion: Maize produces an array of herbivore-induced terpene volatiles that attract parasitoids to infested plants and a suite of pathogen-induced non-volatile terpenoids with antimicrobial activity to defend against pests. Plants rely on complex blends of constitutive and dynamically produced specialized metabolites to mediate beneficial ecological interactions and protect against biotic attack. One such class of metabolites are terpenoids, a large and structurally diverse class of molecules shown to play significant defensive and developmental roles in numerous plant species. Despite this, terpenoids have only recently been recognized as significant contributors to pest resistance in maize (Zea mays), a globally important agricultural crop. The current review details recent advances in our understanding of biochemical structures, pathways and functional roles of maize terpenoids. Dependent upon the lines examined, maize can harbor more than 30 terpene synthases, underlying the inherent diversity of maize terpene defense systems. Part of this defensive arsenal is the inducible production of volatile bouquets that include monoterpenes, homoterpenes and sesquiterpenes, which often function in indirect defense by enabling the attraction of parasitoids and predators. More recently discovered are a subset of sesquiterpene and diterpene hydrocarbon olefins modified by cytochrome P450s to produce non-volatile end-products such kauralexins, zealexins, dolabralexins and β-costic acid. These non-volatile terpenoid phytoalexins often provide effective defense against both microbial and insect pests via direct antimicrobial and anti-feedant activity. The diversity and promiscuity of maize terpene synthases, coupled with a variety of secondary modifications, results in elaborate defensive layers whose identities, regulation and precise functions are continuing to be elucidated.
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http://dx.doi.org/10.1007/s00425-018-2999-2DOI Listing
January 2019

A fragmentation study of isoflavones by IT-TOF-MS using biosynthesized isotopes.

Biosci Biotechnol Biochem 2018 Aug 26;82(8):1309-1315. Epub 2018 Apr 26.

a Graduate School of Agriculture , Kyoto University , Kyoto , Japan.

To aid in the identification and quantification of biologically and agriculturally significant natural products, tandem mass spectrometry can provide accurate structural information with high selectivity and sensitivity. In this study, diagnostic fragmentation patterns of isoflavonoids were examined by liquid chromatography-ion trap-time of flight-mass spectrometry (LC-IT-TOF-MS). The fragmentation scheme for [M+H-2CO] ions derived from isoflavones and [M+H-B-ring-CO] ions derived from 5-hydroxyisoflavones, were investigated using different isotopically labeled isoflavones, specifically [1',2',3',4',5',6',2,3,4-C] and [2',3',5',6',2-D] isoflavones. Specific isotopically labeled isoflavones were prepared through the biosynthetic incorporation of pharmacologically applied C- and D-labelled L-phenylalanine precursors in soybean plants following the application of insect elicitors. Using this approach, we empirically demonstrate that the [M+H-2CO] ion is generated by an intramolecular proton rearrangement during fragmentation. Furthermore, [M+H-B-ring-CO] ion is demonstrated to contain a CH moiety derived from C-ring of 5-hydroxyisoflavones. A mechanistic understanding of characteristic isoflavone fragmentation patterns contributes to the efficacy and confidence in identifying related isoflavones by LC-MS.
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http://dx.doi.org/10.1080/09168451.2018.1465810DOI Listing
August 2018

Discovery, Biosynthesis and Stress-Related Accumulation of Dolabradiene-Derived Defenses in Maize.

Plant Physiol 2018 04 23;176(4):2677-2690. Epub 2018 Feb 23.

Department of Plant Biology, University of California, Davis, California

Terpenoids are a major component of maize () chemical defenses that mediate responses to herbivores, pathogens, and other environmental challenges. Here, we describe the biosynthesis and elicited production of a class of maize diterpenoids, named dolabralexins. Dolabralexin biosynthesis involves the sequential activity of two diterpene synthases, -COPALYL DIPHOSPHATE SYNTHASE (ZmAN2) and KAURENE SYNTHASE-LIKE4 (ZmKSL4). Together, ZmAN2 and ZmKSL4 form the diterpene hydrocarbon dolabradiene. In addition, we biochemically characterized a cytochrome P450 monooxygenase, ZmCYP71Z16, which catalyzes the oxygenation of dolabradiene to yield the epoxides 15,16-epoxydolabrene (epoxydolabrene) and 3β-hydroxy-15,16-epoxydolabrene (epoxydolabranol). The absence of dolabradiene and epoxydolabranol in mutants under elicited conditions confirmed the in vivo biosynthetic requirement of ZmAN2. Combined mass spectrometry and NMR experiments demonstrated that much of the epoxydolabranol is further converted into 3β,15,16-trihydroxydolabrene (trihydroxydolabrene). Metabolite profiling of field-grown maize root tissues indicated that dolabralexin biosynthesis is widespread across common maize cultivars, with trihydroxydolabrene as the predominant diterpenoid. Oxidative stress induced dolabralexin accumulation and transcript expression of and in root tissues, and metabolite and transcript accumulation were up-regulated in response to elicitation with the fungal pathogens and Consistently, epoxydolabranol significantly inhibited the growth of both pathogens in vitro at 10 µg mL, while trihydroxydolabrene-mediated inhibition was specific to These findings suggest that dolabralexins have defense-related roles in maize stress interactions and expand the known chemical space of diterpenoid defenses as genetic targets for understanding and ultimately improving maize resilience.
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http://dx.doi.org/10.1104/pp.17.01351DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5884620PMC
April 2018

Commercial hybrids and mutant genotypes reveal complex protective roles for inducible terpenoid defenses in maize.

J Exp Bot 2018 03;69(7):1693-1705

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, USA.

Plant defense research is facilitated by the use of genome-sequenced inbred lines; however, a foundational knowledge of interactions in commercial hybrids remains relevant to understanding mechanisms present in crops. Using an array of commercial maize hybrids, we quantified the accumulation patterns of defense-related metabolites and phytohormones in tissues challenged with diverse fungal pathogens. Across hybrids, Southern leaf blight (Cochliobolus heterostrophus) strongly elicited specific sesqui- and diterpenoid defenses, namely zealexin A4 (ZA4) and kauralexin diacids, compared with the stalk-rotting agents Fusarium graminearum and Colletotrichum graminicola. With respect to biological activity, ZA4 and kauralexin diacids demonstrated potent antimicrobial action against F. graminearum. Unexpectedly, ZA4 displayed an opposite effect on C. graminicola by promoting growth. Overall, a negative correlation was observed between total analyzed terpenoids and fungal growth. Statistical analyses highlighted kauralexin A3 and abscisic acid as metabolites most associated with fungal suppression. As an empirical test, mutants of the ent-copalyl diphosphate synthase Anther ear 2 (An2) lacking kauralexin biosynthetic capacity displayed increased susceptibility to C. heterostrophus and Fusarium verticillioides. Our results highlight a widely occurring defensive function of acidic terpenoids in commercial hybrids and the complex nature of elicited pathway products that display selective activities on fungal pathogen species.
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http://dx.doi.org/10.1093/jxb/erx495DOI Listing
March 2018

Fungal and herbivore elicitation of the novel maize sesquiterpenoid, zealexin A4, is attenuated by elevated CO.

Planta 2018 Apr;247(4):863-873

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, 92093-0380, USA.

Main Conclusion: Chemical isolation and NMR-based structure elucidation revealed a novel keto-acidic sesquiterpenoid, termed zealexin A4 (ZA4). ZA4 is elicited by pathogens and herbivory, but attenuated by heightened levels of CO . The identification of the labdane-related diterpenoids, termed kauralexins and acidic sesquiterpenoids, termed zealexins, demonstrated the existence of at least ten novel stress-inducible maize metabolites with diverse antimicrobial activity. Despite these advances, the identity of co-occurring and predictably related analytes remains largely unexplored. In the current effort, we identify and characterize the first sesquiterpene keto acid derivative of β-macrocarpene, named zealexin A4 (ZA4). Evaluation of diverse maize inbreds revealed that ZA4 is commonly produced in maize scutella during the first 14 days of seedling development; however, ZA4 production in the scutella was markedly reduced in seedlings grown in sterile soil. Elevated ZA4 production was observed in response to inoculation with adventitious fungal pathogens, such as Aspergillus flavus and Rhizopus microsporus, and a positive relationship between ZA4 production and expression of the predicted zealexin biosynthetic genes, terpene synthases 6 and 11 (Tps6 and Tps11), was observed. ZA4 exhibited significant antimicrobial activity against the mycotoxigenic pathogen A. flavus; however, ZA4 activity against R. microsporus was minimal, suggesting the potential of some fungi to detoxify ZA4. Significant induction of ZA4 production was also observed in response to infestation with the stem tunneling herbivore Ostrinia nubilalis. Examination of the interactive effects of elevated CO (E-CO) on both fungal and herbivore-elicited ZA4 production revealed significantly reduced levels of inducible ZA4 accumulation, consistent with a negative role for E-CO on ZA4 production. Collectively, these results describe a novel β-macrocarpene-derived antifungal defense in maize and expand the established diversity of zealexins that are differentially regulated in response to biotic/abiotic stress.
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http://dx.doi.org/10.1007/s00425-017-2830-5DOI Listing
April 2018

Fungal-induced protein hyperacetylation in maize identified by acetylome profiling.

Proc Natl Acad Sci U S A 2018 01 19;115(1):210-215. Epub 2017 Dec 19.

Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093

Lysine acetylation is a key posttranslational modification that regulates diverse proteins involved in a range of biological processes. The role of histone acetylation in plant defense is well established, and it is known that pathogen effector proteins encoding acetyltransferases can directly acetylate host proteins to alter immunity. However, it is unclear whether endogenous plant enzymes can modulate protein acetylation during an immune response. Here, we investigate how the effector molecule HC-toxin (HCT), a histone deacetylase inhibitor produced by the fungal pathogen race 1, promotes virulence in maize through altering protein acetylation. Using mass spectrometry, we globally quantified the abundance of 3,636 proteins and the levels of acetylation at 2,791 sites in maize plants treated with HCT as well as HCT-deficient or HCT-producing strains of Analyses of these data demonstrate that acetylation is a widespread posttranslational modification impacting proteins encoded by many intensively studied maize genes. Furthermore, the application of exogenous HCT enabled us to show that the activity of plant-encoded enzymes (histone deacetylases) can be modulated to alter acetylation of nonhistone proteins during an immune response. Collectively, these results provide a resource for further mechanistic studies examining the regulation of protein function by reversible acetylation and offer insight into the complex immune response triggered by virulent .
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http://dx.doi.org/10.1073/pnas.1717519115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5776827PMC
January 2018

Selinene Volatiles Are Essential Precursors for Maize Defense Promoting Fungal Pathogen Resistance.

Plant Physiol 2017 Nov 20;175(3):1455-1468. Epub 2017 Sep 20.

Section of Cell and Developmental Biology, University of California San Diego, La Jolla, California 92093-0380

To ensure food security, maize () is a model crop for understanding useful traits underlying stress resistance. In contrast to foliar biochemicals, root defenses limiting the spread of disease remain poorly described. To better understand belowground defenses in the field, we performed root metabolomic profiling and uncovered unexpectedly high levels of the sesquiterpene volatile β-selinene and the corresponding nonvolatile antibiotic derivative β-costic acid. The application of metabolite-based quantitative trait locus mapping using biparental populations, genome-wide association studies, and near-isogenic lines enabled the identification of terpene synthase21 () on chromosome 9 as a β-costic acid pathway candidate gene. Numerous closely examined β-costic acid-deficient inbred lines were found to harbor pseudogenes lacking conserved motifs required for farnesyl diphosphate cyclase activity. For biochemical validation, a full-length was cloned, heterologously expressed in , and demonstrated to cyclize farnesyl diphosphate, yielding β-selinene as the dominant product. Consistent with microbial defense pathways, transcripts strongly accumulate following fungal elicitation. Challenged field roots containing functional alleles displayed β-costic acid levels over 100 μg g fresh weight, greatly exceeding in vitro concentrations required to inhibit the growth of five different fungal pathogens and rootworm larvae (). In vivo disease resistance assays, using and near-isogenic lines, further support the endogenous antifungal role of selinene-derived metabolites. Involved in the biosynthesis of nonvolatile antibiotics, exists as a useful gene for germplasm improvement programs targeting optimized biotic stress resistance.
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http://dx.doi.org/10.1104/pp.17.00879DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664469PMC
November 2017

Biosynthetic pathway of aliphatic formates via a Baeyer-Villiger oxidation in mechanism present in astigmatid mites.

Proc Natl Acad Sci U S A 2017 03 21;114(10):2616-2621. Epub 2017 Feb 21.

Biotechnology Research Center and Department of Biotechnology, Toyama Prefectural University, Imizu, Toyama 939-0398, Japan.

Astigmatid mites depend on bioactive glandular secretions, pheromones, and defensive agents to mediate intra- and interspecies interactions. Aliphatic formates, such as (,)-8,11-heptadecadienyl formate (8,11-F17) and ()-8-heptadecenyl formate (8-F17), are rarely encountered natural products that are abundant in sp. Sasagawa (Acari: Acaridae) mite secretions. Linoleic acid and oleic acid are predicted as key intermediates in the synthesis of the closely related aliphatic formates. To gain insight in this biosynthetic pathway, acarid mite feeding experiments were conducted using C-labeled precursors to precisely track incorporation. Analyses using C NMR spectroscopy demonstrated that the C-labeling pattern of the precursors was detectable on formates in exocrine secretions and likewise on fatty acids in total lipid pools. Curiously, the results demonstrated that the formates were biosynthesized without the dehomologation of corresponding fatty acids. Careful examination of the mass spectra from labeling experiments revealed that the carbonyl carbon of the formates is originally derived from the C-1 position of the fatty acids. Consistent with a Baeyer-Villiger oxidation reaction, labeling studies support the insertion of an oxygen atom between the carbonyl group and carbon chain. Empirical data support the existence of a Baeyer-Villiger monooxygenase responsible for the catalyzation of the Baeyer-Villiger oxidation. The predicted existence of a Baeyer-Villiger monooxygenase capable of converting aliphatic aldehydes to formates represents an exciting opportunity to expand the enzymatic toolbox available for controlled biochemical synthesis.
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http://dx.doi.org/10.1073/pnas.1612611114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5347546PMC
March 2017

Inducible De Novo Biosynthesis of Isoflavonoids in Soybean Leaves by Spodoptera litura Derived Elicitors: Tracer Techniques Aided by High Resolution LCMS.

J Chem Ecol 2016 Dec 8;42(12):1226-1236. Epub 2016 Nov 8.

Graduate School of Agriculture, Kyoto University, Kitashirakawa, Sakyo, Kyoto, Kyoto, 606-8502, Japan.

Isoflavonoids are a characteristic family of natural products in legumes known to mediate a range of plant-biotic interactions. For example, in soybean (Glycine max: Fabaceae) multiple isoflavones are induced and accumulate in leaves following attack by Spodoptera litura (Lepidoptera: Noctuidae) larvae. To quantitatively examine patterns of activated de novo biosynthesis, soybean (Var. Enrei) leaves were treated with a combination of plant defense elicitors present in S. litura gut content extracts and L-α-[C, N]phenylalanine as a traceable isoflavonoid precursor. Combined treatments promoted significant increases in C-labeled isoflavone aglycones (daidzein, formononetin, and genistein), C-labeled isoflavone 7-O-glucosides (daidzin, ononin, and genistin), and C-labeled isoflavone 7-O-(6″-O-malonyl-β-glucosides) (malonyldaidzin, malonylononin, and malonylgenistin). In contrast levels of C-labeled flavones and flavonol (4',7-dihydroxyflavone, kaempferol, and apigenin) were not significantly altered. Curiously, application of fatty acid-amino acid conjugate (FAC) elicitors present in S. litura gut contents, namely N-linolenoyl-L-glutamine and N-linoleoyl-L-glutamine, both promoted the induced accumulation of isoflavone 7-O-glucosides and isoflavone 7-O-(6″-O-malonyl-β-glucosides), but not isoflavone aglycones in the leaves. These results demonstrate that at least two separate reactions are involved in elicitor-induced soybean leaf responses to the S. litura gut contents: one is the de novo biosynthesis of isoflavone conjugates induced by FACs, and the other is the hydrolysis of the isoflavone conjugates to yield isoflavone aglycones. Gut content extracts alone displayed no hydrolytic activity. The quantitative analysis of isoflavone de novo biosynthesis, with respect to both aglycones and conjugates, affords a useful bioassay system for the discovery of additional plant defense elicitor(s) in S. litura gut contents that specifically promote hydrolysis of isoflavone conjugates.
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http://dx.doi.org/10.1007/s10886-016-0786-8DOI Listing
December 2016

Interactive Effects of Elevated [CO2] and Drought on the Maize Phytochemical Defense Response against Mycotoxigenic Fusarium verticillioides.

PLoS One 2016 13;11(7):e0159270. Epub 2016 Jul 13.

Chemistry Research Unit, Center of Medical, Agricultural, and Veterinary Entomology, United States Department of Agriculture, Agricultural Research Service, 1600 SW 23rd Drive, Gainesville, Florida, 32608, United States of America.

Changes in climate due to rising atmospheric carbon dioxide concentration ([CO2]) are predicted to intensify episodes of drought, but our understanding of how these combined conditions will influence crop-pathogen interactions is limited. We recently demonstrated that elevated [CO2] alone enhances maize susceptibility to the mycotoxigenic pathogen, Fusarium verticillioides (Fv) but fumonisin levels remain unaffected. In this study we show that maize simultaneously exposed to elevated [CO2] and drought are even more susceptible to Fv proliferation and also prone to higher levels of fumonisin contamination. Despite the increase in fumonisin levels, the amount of fumonisin produced in relation to pathogen biomass remained lower than corresponding plants grown at ambient [CO2]. Therefore, the increase in fumonisin contamination was likely due to even greater pathogen biomass rather than an increase in host-derived stimulants. Drought did not negate the compromising effects of elevated [CO2] on the accumulation of maize phytohormones and metabolites. However, since elevated [CO2] does not influence the drought-induced accumulation of abscisic acid (ABA) or root terpenoid phytoalexins, the effects elevated [CO2] are negated belowground, but the stifled defense response aboveground may be a consequence of resource redirection to the roots.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0159270PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943682PMC
August 2017

A maize death acid, 10-oxo-11-phytoenoic acid, is the predominant cyclopentenone signal present during multiple stress and developmental conditions.

Plant Signal Behav 2016 ;11(2):e1120395

b Section of Cell and Developmental Biology, University of California at San Diego , La Jolla , CA , USA.

Recently we investigated the function of the 9-lipoxygenase (LOX) derived cyclopentenones 10-oxo-11-phytoenoic acid (10-OPEA) and 10-oxo-11,15-phytodienoic acid (10-OPDA) and identified their C-14 and C-12 derivatives. 10-OPEA accumulation is elicited by fungal and insect attack and acts as a strong inhibitor of microbial and herbivore growth. Although structurally similar, comparative analyses between 10-OPEA and its 13-LOX analog 12-oxo-phytodienoic acid (12-OPDA) demonstrate specificity in transcript accumulation linked to detoxification, secondary metabolism, jasmonate regulation, and protease inhibition. As a potent cell death signal, 10-OPEA activates cysteine protease activity leading to ion leakage and apoptotic-like DNA fragmentation. In this study we further elucidate the distribution, abundance, and functional roles of 10-OPEA, 10-OPDA, and 12-OPDA, in diverse organs under pathogen- and insect-related stress.
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http://dx.doi.org/10.1080/15592324.2015.1120395DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4883972PMC
December 2016

Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays.

Plant Physiol 2015 Nov 16;169(3):1727-43. Epub 2015 Sep 16.

Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.)

As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.
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http://dx.doi.org/10.1104/pp.15.01039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4634079PMC
November 2015

Maize death acids, 9-lipoxygenase-derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators.

Proc Natl Acad Sci U S A 2015 Sep 24;112(36):11407-12. Epub 2015 Aug 24.

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093-0380;

Plant damage promotes the interaction of lipoxygenases (LOXs) with fatty acids yielding 9-hydroperoxides, 13-hydroperoxides, and complex arrays of oxylipins. The action of 13-LOX on linolenic acid enables production of 12-oxo-phytodienoic acid (12-OPDA) and its downstream products, termed "jasmonates." As signals, jasmonates have related yet distinct roles in the regulation of plant resistance against insect and pathogen attack. A similar pathway involving 9-LOX activity on linolenic and linoleic acid leads to the 12-OPDA positional isomer, 10-oxo-11-phytodienoic acid (10-OPDA) and 10-oxo-11-phytoenoic acid (10-OPEA), respectively; however, physiological roles for 9-LOX cyclopentenones have remained unclear. In developing maize (Zea mays) leaves, southern leaf blight (Cochliobolus heterostrophus) infection results in dying necrotic tissue and the localized accumulation of 10-OPEA, 10-OPDA, and a series of related 14- and 12-carbon metabolites, collectively termed "death acids." 10-OPEA accumulation becomes wound inducible within fungal-infected tissues and at physiologically relevant concentrations acts as a phytoalexin by suppressing the growth of fungi and herbivores including Aspergillus flavus, Fusarium verticillioides, and Helicoverpa zea. Unlike previously established maize phytoalexins, 10-OPEA and 10-OPDA display significant phytotoxicity. Both 12-OPDA and 10-OPEA promote the transcription of defense genes encoding glutathione S transferases, cytochrome P450s, and pathogenesis-related proteins. In contrast, 10-OPEA only weakly promotes the accumulation of multiple protease inhibitor transcripts. Consistent with a role in dying tissue, 10-OPEA application promotes cysteine protease activation and cell death, which is inhibited by overexpression of the cysteine protease inhibitor maize cystatin-9. Unlike jasmonates, functions for 10-OPEA and associated death acids are consistent with specialized roles in local defense reactions.
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http://dx.doi.org/10.1073/pnas.1511131112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4568653PMC
September 2015

Impacts of insect oral secretions on defoliation-induced plant defense.

Authors:
Eric A Schmelz

Curr Opin Insect Sci 2015 Jun 18;9:7-15. Epub 2015 Apr 18.

Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA 92093-0380, United States. Electronic address:

Plant responses to biotic stress involve non-self perception, signaling, and altered defense phenotypes. During attack, defoliating insects deposit gland secretions (GS) and complex foregut derived oral secretions (OS) that include GS and combined products of plant, insect, and microbial interactions. GS-derived and OS-derived biochemicals that trigger defense are termed Herbivore Associated Molecular Patterns (HAMPs) while those that promote susceptibility are termed effectors. These functions are highly context and species specific. The magnitude and direction of plant responses are orchestrated by the interaction of damage, OS/GS components, predicted receptor-ligand interactions, ion fluxes, protein kinase signaling cascades, phytohormone interactions, transcription factor activation, altered translation, and defense biosynthesis. Unlike plant-pathogen recognition, a remaining challenge is the discovery of plant receptors for defoliator-derived HAMPs.
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http://dx.doi.org/10.1016/j.cois.2015.04.002DOI Listing
June 2015

Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance.

Plant Cell Environ 2015 Nov 23;38(11):2195-207. Epub 2015 Jan 23.

Chemistry Research Unit, Center of Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service, United States Department of Agriculture, Gainesville, FL, 32608, USA.

Maize (Zea mays) production, which is of global agro-economic importance, is largely limited by herbivore pests, pathogens and environmental conditions, such as drought. Zealexins and kauralexins belong to two recently identified families of acidic terpenoid phytoalexins in maize that mediate defence against both pathogen and insect attacks in aboveground tissues. However, little is known about their function in belowground organs and their potential to counter abiotic stress. In this study, we show that zealexins and kauralexins accumulate in roots in response to both biotic and abiotic stress including, Diabrotica balteata herbivory, Fusarium verticillioides infection, drought and high salinity. We find that the quantity of drought-induced phytoalexins is positively correlated with the root-to-shoot ratio of different maize varieties, and further demonstrate that mutant an2 plants deficient in kauralexin production are more sensitive to drought. The induction of phytoalexins in response to drought is root specific and does not influence phytoalexin levels aboveground; however, the accumulation of phytoalexins in one tissue may influence the induction capacity of other tissues.
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http://dx.doi.org/10.1111/pce.12482DOI Listing
November 2015

Accumulation of 5-hydroxynorvaline in maize (Zea mays) leaves is induced by insect feeding and abiotic stress.

J Exp Bot 2015 Feb 30;66(2):593-602. Epub 2014 Sep 30.

Boyce Thompson Institute for Plant Research, Ithaca, NY, USA.

Plants produce a wide variety of defensive metabolites to protect themselves against herbivores and pathogens. Non-protein amino acids, which are present in many plant species, can have a defensive function through their mis-incorporation during protein synthesis and/or inhibition of biosynthetic pathways in primary metabolism. 5-Hydroxynorvaline was identified in a targeted search for previously unknown non-protein amino acids in the leaves of maize (Zea mays) inbred line B73. Accumulation of this compound increases during herbivory by aphids (Rhopalosiphum maidis, corn leaf aphid) and caterpillars (Spodoptera exigua, beet armyworm), as well as in response to treatment with the plant signalling molecules methyl jasmonate, salicylic acid and abscisic acid. In contrast, ethylene signalling reduced 5-hydroxynorvaline abundance. Drought stress induced 5-hydroxynorvaline accumulation to a higher level than insect feeding or treatment with defence signalling molecules. In field-grown plants, the 5-hydroxynorvaline concentration was highest in above-ground vegetative tissue, but it was also detectable in roots and dry seeds. When 5-hydroxynorvaline was added to aphid artificial diet at concentrations similar to those found in maize leaves and stems, R. maidis reproduction was reduced, indicating that this maize metabolite may have a defensive function. Among 27 tested maize inbred lines there was a greater than 10-fold range in the accumulation of foliar 5-hydroxynorvaline. Genetic mapping populations derived from a subset of these inbred lines were used to map quantitative trait loci for 5-hydroxynorvaline accumulation to maize chromosomes 5 and 7.
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http://dx.doi.org/10.1093/jxb/eru385DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4286406PMC
February 2015

The novel monocot-specific 9-lipoxygenase ZmLOX12 is required to mount an effective jasmonate-mediated defense against Fusarium verticillioides in maize.

Mol Plant Microbe Interact 2014 Nov;27(11):1263-76

Fusarium verticillioides is a major limiting factor for maize production due to ear and stalk rot and the contamination of seed with the carcinogenic mycotoxin fumonisin. While lipoxygenase (LOX)-derived oxylipins have been implicated in defense against diverse pathogens, their function in maize resistance against F. verticillioides is poorly understood. Here, we functionally characterized a novel maize 9-LOX gene, ZmLOX12. This gene is distantly related to known dicot LOX genes, with closest homologs found exclusively in other monocot species. ZmLOX12 is predominantly expressed in mesocotyls in which it is strongly induced in response to F. verticillioides infection. The Mutator transposon-insertional lox12-1 mutant is more susceptible to F. verticillioides colonization of mesocotyls, stalks, and kernels. The infected mutant kernels accumulate a significantly greater amount of the mycotoxin fumonisin. Reduced resistance to the pathogen is accompanied by diminished levels of the jasmonic acid (JA) precursor 12-oxo phytodienoic acid, JA-isoleucine, and expression of jasmonate-biosynthetic genes. Supporting the strong defense role of jasmonates, the JA-deficient opr7 opr8 double mutant displayed complete lack of immunity to F. verticillioides. Unexpectedly, the more susceptible lox12 mutant accumulated higher levels of kauralexins, suggesting that F. verticillioides is tolerant to this group of antimicrobial phytoalexins. This study demonstrates that this unique monocot-specific 9-LOX plays a key role in defense against F. verticillioides in diverse maize tissues and provides genetic evidence that JA is the major defense hormone against this pathogen.
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http://dx.doi.org/10.1094/MPMI-06-13-0184-RDOI Listing
November 2014

Insect-induced daidzein, formononetin and their conjugates in soybean leaves.

Metabolites 2014 Jul 4;4(3):532-46. Epub 2014 Jul 4.

Graduate School of Agriculture, Kyoto University, Kitashirakawa, Sakyo, Kyoto 606-8502, Japan.

In response to attack by bacterial pathogens, soybean (Gylcine max) leaves accumulate isoflavone aglucones, isoflavone glucosides, and glyceollins. In contrast to pathogens, the dynamics of related insect-inducible metabolites in soybean leaves remain poorly understood. In this study, we analyzed the biochemical responses of soybean leaves to Spodoptera litura (Lepidoptera: Noctuidae) herbivory and also S. litura gut contents, which contain oral secretion elicitors. Following S. litura herbivory, soybean leaves displayed an induced accumulation of the flavone and isoflavone aglycones 4',7-dihyroxyflavone, daidzein, and formononetin, and also the isoflavone glucoside daidzin. Interestingly, foliar application of S. litura oral secretions also elicited the accumulation of isoflavone aglycones (daidzein and formononetin), isoflavone 7-O-glucosides (daidzin, ononin), and isoflavone 7-O-(6'-O-malonyl-β-glucosides) (malonyldaidzin, malonylononin). Consistent with the up-regulation of the isoflavonoid biosynthetic pathway, folair phenylalanine levels also increased following oral secretion treatment. To establish that these metabolitic changes were the result of de novo biosynthesis, we demonstrated that labeled (13C9) phenylalanine was incorporated into the isoflavone aglucones. These results are consistent with the presence of soybean defense elicitors in S. litura oral secretions. We demonstrate that isoflavone aglycones and isoflavone conjugates are induced in soybean leaves, not only by pathogens as previously demonstrated, but also by foliar insect herbivory.
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http://dx.doi.org/10.3390/metabo4030532DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4192678PMC
July 2014

Influence of brown stink bug feeding, planting date and sampling time on common smut infection of maize.

Insect Sci 2014 Oct 20;21(5):564-71. Epub 2014 Aug 20.

USDA-ARS, Crop Genetics and Breeding Research Unit, Tifton, GA, 31793.

Phytopathogen infections are frequently influenced by both biotic and abiotic factors in a crop field. The effect of brown stink bug, Euschistus servus (Hemiptera: Pentatomidae), feeding and planting date and sampling time on common smut (Ustilago maydis) infection percentage of maize plants was examined in 2005 and 2006, and 2010 and 2011, respectively. Brown stink bug adult feeding on maize hybrid "DKC6971" at flowering in 2005 and 2006 did not influence smut infection percentage when examined using 3 treatments (i.e., 0 adult, 5 adults, and 5 adults mixed with the smut spores). The smut infection percentages were <3% (n = 12) in the 3 treatments. The smut infection percentage among the 4 weekly samplings was the same, so was natural aflatoxin contamination at harvest among the treatments. The 2nd experiment showed that planting date did not affect the smut infection percentage in either 2010 or 2011. But, the smut infection percentage from the postflowering sampling was greater than preflowering sampling in both years. The smut infection percentage varied among the germplasm lines in 2010, but not in 2011. This study demonstrated that brown stink bug feeding at flowering had no effect on smut infection in maize, and the best time for smut evaluation would be after flowering. The temperature and precipitation might have also influenced the percentage of smut-infected maize plants during the 4 years when the experiments were conducted. The similarity between kernel-colonizing U. maydis and Aspergillus flavus infections and genotype × environment interaction were also discussed.
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http://dx.doi.org/10.1111/1744-7917.12149DOI Listing
October 2014

Effects of elevated [CO2 ] on maize defence against mycotoxigenic Fusarium verticillioides.

Plant Cell Environ 2014 Dec 13;37(12):2691-706. Epub 2014 May 13.

Chemistry Research Unit, Center of Medical, Agricultural, and Veterinary Entomology, U.S. Department of Agriculture, Agricultural Research Service, Gainesville, FL, 32608, USA.

Maize is by quantity the most important C4 cereal crop; however, future climate changes are expected to increase maize susceptibility to mycotoxigenic fungal pathogens and reduce productivity. While rising atmospheric [CO2 ] is a driving force behind the warmer temperatures and drought, which aggravate fungal disease and mycotoxin accumulation, our understanding of how elevated [CO2 ] will effect maize defences against such pathogens is limited. Here we report that elevated [CO2 ] increases maize susceptibility to Fusarium verticillioides proliferation, while mycotoxin levels are unaltered. Fumonisin production is not proportional to the increase in F. verticillioides biomass, and the amount of fumonisin produced per unit pathogen is reduced at elevated [CO2 ]. Following F. verticillioides stalk inoculation, the accumulation of sugars, free fatty acids, lipoxygenase (LOX) transcripts, phytohormones and downstream phytoalexins is dampened in maize grown at elevated [CO2 ]. The attenuation of maize 13-LOXs and jasmonic acid production correlates with reduced terpenoid phytoalexins and increased susceptibility. Furthermore, the attenuated induction of 9-LOXs, which have been suggested to stimulate mycotoxin biosynthesis, is consistent with reduced fumonisin per unit fungal biomass at elevated [CO2 ]. Our findings suggest that elevated [CO2 ] will compromise maize LOX-dependent signalling, which will influence the interactions between maize and mycotoxigenic fungi.
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http://dx.doi.org/10.1111/pce.12337DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4278449PMC
December 2014

Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins.

Plant J 2014 Aug 26;79(4):659-78. Epub 2014 Mar 26.

Center for Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture, Agricultural Research Service, Chemistry Research Unit, Gainesville, FL, 32608, USA.

A long-standing goal in plant research is to optimize the protective function of biochemical agents that impede pest and pathogen attack. Nearly 40 years ago, pathogen-inducible diterpenoid production was described in rice, and these compounds were shown to function as antimicrobial phytoalexins. Using rice and maize as examples, we discuss recent advances in the discovery, biosynthesis, elicitation and functional characterization of monocot terpenoid phytoalexins. The recent expansion of known terpenoid phytoalexins now includes not only the labdane-related diterpenoid superfamily but also casbane-type diterpenoids and β-macrocarpene-derived sequiterpenoids. Biochemical approaches have been used to pair pathway precursors and end products with cognate biosynthetic genes. The number of predicted terpenoid phytoalexins is expanding through advances in cereal genome annotation and terpene synthase characterization that likewise enable discoveries outside the Poaceae. At the cellular level, conclusive evidence now exists for multiple plant receptors of fungal-derived chitin elicitors, phosphorylation of membrane-associated signaling complexes, activation of mitogen-activated protein kinase, involvement of phytohormone signals, and the existence of transcription factors that mediate the expression of phytoalexin biosynthetic genes and subsequent accumulation of pathway end products. Elicited production of terpenoid phytoalexins exhibit additional biological functions, including root exudate-mediated allelopathy and insect antifeedant activity. Such findings have encouraged consideration of additional interactions that blur traditionally discrete phytoalexin classifications. The establishment of mutant collections and increasing ease of genetic transformation assists critical examination of further biological roles. Future research directions include examination of terpenoid phytoalexin precursors and end products as potential signals mediating plant physiological processes.
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http://dx.doi.org/10.1111/tpj.12436DOI Listing
August 2014

Head-group acylation of monogalactosyldiacylglycerol is a common stress response, and the acyl-galactose acyl composition varies with the plant species and applied stress.

Physiol Plant 2014 Apr 27;150(4):517-28. Epub 2013 Dec 27.

Kansas Lipidomics Research Center, Division of Biology, Ackert Hall, Kansas State University, Manhattan, KS, 66506, USA.

Formation of galactose-acylated monogalactosyldiacylglycerols has been shown to be induced by leaf homogenization, mechanical wounding, avirulent bacterial infection and thawing after snap-freezing. Here, lipidomic analysis using mass spectrometry showed that galactose-acylated monogalactosyldiacylglycerols, formed in wheat (Triticum aestivum) and tomato (Solanum lycopersicum) leaves upon wounding, have acyl-galactose profiles that differ from those of wounded Arabidopsis thaliana, indicating that different plant species accumulate different acyl-galactose components in response to the same stress. Additionally, the composition of the acyl-galactose component of Arabidopsis acMGDG (galactose-acylated monogalactosyldiacylglycerol) depends on the stress treatment. After sub-lethal freezing treatment, acMGDG contained mainly non-oxidized fatty acids esterified to galactose, whereas mostly oxidized fatty acids accumulated on galactose after wounding or bacterial infection. Compositional data are consistent with acMGDG being formed in vivo by transacylation with fatty acids from digalactosyldiacylglycerols. Oxophytodienoic acid, an oxidized fatty acid, was more concentrated on the galactosyl ring of acylated monogalactosyldiacylglycerols than in galactolipids in general. Also, oxidized fatty acid-containing acylated monogalactosyldiacylglycerols increased cumulatively when wounded Arabidopsis leaves were wounded again. These findings suggest that, in Arabidopsis, the pool of galactose-acylated monogalactosyldiacylglycerols may serve to sequester oxidized fatty acids during stress responses.
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http://dx.doi.org/10.1111/ppl.12132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3954903PMC
April 2014
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