Publications by authors named "Shawn A Christensen"

33 Publications

Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize.

Mol Plant Pathol 2021 Apr 28;22(4):465-479. Epub 2021 Feb 28.

Department of Entomology and Plant Pathology, NC State University, Raleigh, North Carolina, USA.

Common rust, caused by Puccinia sorghi, is a widespread and destructive disease of maize. The Rp1-D gene confers resistance to the P. sorghi IN2 isolate, mediating a hypersensitive cell death response (HR). To identify differentially expressed genes (DEGs) and metabolites associated with the compatible (susceptible) interaction and with Rp1-D-mediated resistance in maize, we performed transcriptomics and targeted metabolome analyses of P. sorghi IN2-infected leaves from the near-isogenic lines H95 and H95:Rp1-D, which differed for the presence of Rp1-D. We observed up-regulation of genes involved in the defence response and secondary metabolism, including the phenylpropanoid, flavonoid, and terpenoid pathways. Metabolome analyses confirmed that intermediates from several transcriptionally up-regulated pathways accumulated during the defence response. We identified a common response in H95:Rp1-D and H95 with an additional H95:Rp1-D-specific resistance response observed at early time points at both transcriptional and metabolic levels. To better understand the mechanisms underlying Rp1-D-mediated resistance, we inferred gene regulatory networks occurring in response to P. sorghi infection. A number of transcription factors including WRKY53, BHLH124, NKD1, BZIP84, and MYB100 were identified as potentially important signalling hubs in the resistance-specific response. Overall, this study provides a novel and multifaceted understanding of the maize susceptible and resistance-specific responses to P. sorghi.
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http://dx.doi.org/10.1111/mpp.13040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7938627PMC
April 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

Metabolomics by UHPLC-HRMS reveals the impact of heat stress on pathogen-elicited immunity in maize.

Metabolomics 2021 01 5;17(1). Epub 2021 Jan 5.

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

Introduction: Studies investigating crop resistance to abiotic and biotic stress have largely focused on plant responses to singular forms of stress and individual biochemical pathways that only partially represent stress responses. Thus, combined abiotic and biotic stress treatments and the global assessment of their elicited metabolic expression remains largely unexplored. In this study, we employed targeted and untargeted metabolomics to investigate the molecular responses of maize (Zea mays) to abiotic, biotic, and combinatorial stress.

Objective: We compared the inducible metabolomes of heat-stressed (abiotic) and C. heterostrophus-infected (biotic) maize and examined the effects of heat stress on the ability of maize to defend itself against C. heterostrophus.

Methods: Ultra-high-performance liquid chromatography-high-resolution mass spectrometry was performed on plants grown under control conditions (28 °C), heat stress (38 °C), Cochliobolus heterostrophus infection, or combinatorial stress [heat (38 °C) + C. heterostrophus infection].

Results: Multivariate analyses revealed differential metabolite expression between heat stress, C. heterostrophus infection, and their respective controls. In combinatorial experiments, treatment with heat stress prior to fungal inoculation negatively impacted maize disease resistance against C. heterostrophus, and distinct metabolome separation between combinatorial stressed plants and the non-heat-stressed infected controls was observed. Targeted analysis revealed inducible primary and secondary metabolite responses to abiotic/biotic stress, and combinatorial experiments indicated that deficiency in the hydroxycinnamic acid, p-coumaric acid, may contribute to the heat-induced susceptibility of maize to C. heterostrophus.

Conclusion: These findings demonstrate that abiotic stress can predispose crops to more severe disease symptoms, underlining the increasing need to investigate defense chemistry in plants under combinatorial stress.
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http://dx.doi.org/10.1007/s11306-020-01739-2DOI Listing
January 2021

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

The 13-lipoxygenase MSD2 and the ω-3 fatty acid desaturase MSD3 impact Spodoptera frugiperda resistance in Sorghum.

Planta 2020 Sep 23;252(4):62. Epub 2020 Sep 23.

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

Main Conclusion: Linolenic acid produced by the ω-3 fatty acid desaturase MSD3 in sorghum is used for insect-induced jasmonic acid production and is important for resistance against Spodoptera frugiperda. Jasmonic acid (JA) is a phytohormone that regulates both plant development and stress responses. In sorghum (Sorghum bicolor), the ω-3 fatty acid desaturase Multiseeded3 (MSD3) and the 13-lipoxygenase Multiseeded2 (MSD2) are important for producing JA to regulate panicle development and spikelet fertility, but their function in plant defense remains unknown. In this study, we examined whether these genes are important for the production of JA in response to herbivory by the insect pest Spodoptera frugiperda. Compared to wild-type controls, the msd3 mutant accumulated less JA in leaves of both infested and uninfested plants, revealing that MSD3 is involved in stress-induced JA production. In contrast, herbivore-induced JA production in the msd2 mutant was indistinguishable from wild type, indicating that MSD2 does not function in herbivore-induced JA production. An increase of S. frugiperda growth was observed on both the msd3 and msd2 mutants, hinting at roles for both JA and additional oxylipins in sorghum's defense responses.
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http://dx.doi.org/10.1007/s00425-020-03475-2DOI Listing
September 2020

Green leaf volatiles and jasmonic acid enhance susceptibility to anthracnose diseases caused by Colletotrichum graminicola in maize.

Mol Plant Pathol 2020 05 27;21(5):702-715. Epub 2020 Feb 27.

Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, USA.

Colletotrichum graminicola is a hemibiotrophic fungus that causes anthracnose leaf blight (ALB) and anthracnose stalk rot (ASR) in maize. Despite substantial economic losses caused by these diseases, the defence mechanisms against this pathogen remain poorly understood. Several hormones are suggested to aid in defence against C. graminicola, such as jasmonic acid (JA) and salicylic acid (SA), but supporting genetic evidence was not reported. Green leaf volatiles (GLVs) are a group of well-characterized volatiles that induce JA biosynthesis in maize and are known to function in defence against necrotrophic pathogens. Information regarding the role of GLVs and JA in interactions with (hemi)biotrophic pathogens remains limited. To functionally elucidate GLVs and JA in defence against a hemibiotrophic pathogen, we tested GLV- and JA-deficient mutants, lox10 and opr7 opr8, respectively, for resistance to ASR and ALB and profiled jasmonates and SA in their stalks and leaves throughout infection. Both mutants were resistant and generally displayed elevated levels of SA and low amounts of jasmonates, especially at early stages of infection. Pretreatment with GLVs restored susceptibility of lox10 mutants, but not opr7 opr8 mutants, which coincided with complete rescue of JA levels. Exogenous methyl jasmonate restored susceptibility in both mutants when applied before inoculation, whereas methyl salicylate did not induce further resistance in either of the mutants, but did induce mutant-like resistance in the wild type. Collectively, this study reveals that GLVs and JA contribute to maize susceptibility to C. graminicola due to suppression of SA-related defences.
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http://dx.doi.org/10.1111/mpp.12924DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7170777PMC
May 2020

Setaria viridis as a model for translational genetic studies of jasmonic acid-related insect defenses in Zea mays.

Plant Sci 2020 Feb 12;291:110329. Epub 2019 Nov 12.

Chemistry Research Unit, USDA Agricultural Research Service, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, FL, 32608, USA.

Little is known regarding insect defense pathways in Setaria viridis (setaria), a model system for panicoid grasses, including Zea mays (maize). It is thus of interest to compare insect herbivory responses of setaria and maize. Here we use metabolic, phylogenetic, and gene expression analyses to measure a subset of jasmonic acid (JA)-related defense responses to leaf-chewing caterpillars. Phylogenetic comparisons of known defense-related maize genes were used to identify putative orthologs in setaria, and candidates were tested by quantitative PCR to determine transcriptional responses to insect challenge. Our findings show that while much of the core JA-related metabolic and genetic responses appear conserved between setaria and maize, production of downstream secondary metabolites such as benzoxazinoids and herbivore-induced plant volatiles are dissimilar. This diversity of chemical defenses and gene families involved in secondary metabolism among grasses presents new opportunities for cross species engineering. The high degree of genetic similarity and ease of orthologous gene identification between setaria and maize make setaria an excellent species for translational genetic studies, but the species specificity of downstream insect defense chemistry makes some pathways unamenable to cross-species comparisons.
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http://dx.doi.org/10.1016/j.plantsci.2019.110329DOI Listing
February 2020

Sorghum Encodes an ω-3 Fatty Acid Desaturase that Increases Grain Number by Reducing Jasmonic Acid Levels.

Int J Mol Sci 2019 Oct 28;20(21). Epub 2019 Oct 28.

Plant Stress and Germplasm Development Unit, Cropping Systems Research Laboratory, U.S. Department of Agriculture-Agricultural Research Service, Lubbock, TX 79415, USA.

Grain number per panicle is an important component of grain yield in sorghum ( (L.)) and other cereal crops. Previously, we reported that mutations in multi-seeded 1 ( and genes result in a two-fold increase in grain number per panicle due to the restoration of the fertility of the pedicellate spikelets, which invariably abort in natural sorghum accessions. Here, we report the identification of another gene, which is also involved in the regulation of grain numbers in sorghum. Four bulked F populations from crosses between BTx623 and each of the independent mutants p6, p14, p21, and p24 were sequenced to 20× coverage of the whole genome on a HiSeq 2000 system. Bioinformatic analyses of the sequence data showed that one gene, Sorbi_3001G407600, harbored homozygous mutations in all four populations. This gene encodes a plastidial ω-3 fatty acid desaturase that catalyzes the conversion of linoleic acid (18:2) to linolenic acid (18:3), a substrate for jasmonic acid (JA) biosynthesis. The mutants had reduced levels of linolenic acid in both leaves and developing panicles that in turn decreased the levels of JA. Furthermore, the panicle phenotype was reversed by treatment with methyl-JA (MeJA). Our characterization of and now demonstrates that JA-regulated processes are critical to the phenotype. The identification of the gene reveals a new target that could be manipulated to increase grain number per panicle in sorghum, and potentially other cereal crops, through the genomic editing of functional orthologs.
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http://dx.doi.org/10.3390/ijms20215359DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6862555PMC
October 2019

Fertility of Pedicellate Spikelets in Sorghum Is Controlled by a Jasmonic Acid Regulatory Module.

Int J Mol Sci 2019 Oct 8;20(19). Epub 2019 Oct 8.

Plant Stress and Germplasm Development Unit, Cropping Systems Research Laboratory, U.S. Department of Agriculture-Agricultural Research Service, Lubbock, TX 79415, USA.

As in other cereal crops, the panicles of sorghum ( (L.) Moench) comprise two types of floral spikelets (grass flowers). Only sessile spikelets (SSs) are capable of producing viable grains, whereas pedicellate spikelets (PSs) cease development after initiation and eventually abort. Consequently, grain number per panicle (GNP) is lower than the total number of flowers produced per panicle. The mechanism underlying this differential fertility is not well understood. To investigate this issue, we isolated a series of ethyl methane sulfonate (EMS)-induced () mutants that result in full spikelet fertility, effectively doubling GNP. Previously, we showed that MSD1 is a TCP (Teosinte branched/Cycloidea/PCF) transcription factor that regulates jasmonic acid (JA) biosynthesis, and ultimately floral sex organ development. Here, we show that encodes a lipoxygenase (LOX) that catalyzes the first committed step of JA biosynthesis. Further, we demonstrate that MSD1 binds to the promoters of and other JA pathway genes. Together, these results show that a JA-induced module regulates sorghum panicle development and spikelet fertility. The findings advance our understanding of inflorescence development and could lead to new strategies for increasing GNP and grain yield in sorghum and other cereal crops.
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http://dx.doi.org/10.3390/ijms20194951DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6801740PMC
October 2019

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

Fighting on two fronts: Elevated insect resistance in flooded maize.

Plant Cell Environ 2020 01 22;43(1):223-234. Epub 2019 Aug 22.

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

To grow and thrive plants must be able to adapt to both adverse environmental conditions and attack by a variety of pests. Elucidating the sophisticated mechanisms plants have developed to achieve this has been the focus of many studies. What is less well understood is how plants respond when faced with multiple stressors simultaneously. In this study, we assess the response of Zea mays (maize) to the combinatorial stress of flooding and infestation with the insect pest Spodoptera frugiperda (fall armyworm). This combined stress leads to elevated production of the defence hormone salicylic acid, which does not occur in the individual stresses, and the resultant salicylic acid-dependent increase in S. frugiperda resistance. Remodelling of phenylpropanoid pathways also occurs in response to this combinatorial stress leading to increased production of the anti-insect C-glycosyl flavones (maysins) and the herbivore-induced volatile phenolics, benzyl acetate, and phenethyl acetate. Furthermore, changes in cellular redox status also occur, as indicated by reductions in peroxidase and polyphenol oxidase activity. These data suggest that metabolite changes important for flooding tolerance and anti-insect defence may act both additively and synergistically to provide extra protection to the plant.
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http://dx.doi.org/10.1111/pce.13642DOI Listing
January 2020

A maize polygalacturonase functions as a suppressor of programmed cell death in plants.

BMC Plant Biol 2019 Jul 15;19(1):310. Epub 2019 Jul 15.

Dept. of Entomology and Plant Pathology, NC State University, Raleigh, NC, 27695-7616, USA.

Background: The hypersensitive defense response (HR) in plants is a fast, localized necrotic response around the point of pathogen ingress. HR is usually triggered by a pathogen recognition event mediated by a nucleotide-binding site, leucine-rich repeat (NLR) protein. The autoactive maize NLR gene Rp1-D21 confers a spontaneous HR response in the absence of pathogen recognition. Previous work identified a set of loci associated with variation in the strength of Rp1-D21-induced HR. A polygalacturonase gene homolog, here termed ZmPGH1, was identified as a possible causal gene at one of these loci on chromosome 7.

Results: Expression of ZmPGH1 inhibited the HR-inducing activity of both Rp1-D21 and that of another autoactive NLR, RPM1(D505V), in a Nicotiana benthamiana transient expression assay system. Overexpression of ZmPGH1 in a transposon insertion line of maize was associated with suppression of chemically-induced programmed cell death and with suppression of HR induced by Rp1-D21 in maize plants grown in the field.

Conclusions: ZmPGH1 functions as a suppressor of programmed cell death induced by at least two autoactive NLR proteins and by two chemical inducers. These findings deepen our understanding of the control of the HR in plants.
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http://dx.doi.org/10.1186/s12870-019-1897-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6628502PMC
July 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

Interactions Among Plants, Insects, and Microbes: Elucidation of Inter-Organismal Chemical Communications in Agricultural Ecology.

J Agric Food Chem 2018 Jul 25;66(26):6663-6674. Epub 2018 Jun 25.

Center for Chemical Ecology , Penn State University , University Park , Pennsylvania 16802 , United States.

The last 2 decades have witnessed a sustained increase in the study of plant-emitted volatiles and their role in plant-insect, plant-microbe, and plant-plant interactions. While each of these binary systems involves complex chemical and biochemical processes between two organisms, the progression of increasing complexity of a ternary system (i.e., plant-insect-microbe), and the study of a ternary system requires nontrivial planning. This planning can include an experimental design that factors in potential overarching ecological interactions regarding the binary or ternary system, correctly identifying and understanding unexpected observations that may occur during the experiment and thorough interpretation of the resultant data. This challenge of planning, performing, and interpreting a plant's defensive response to multiple biotic stressors will be even greater when abiotic stressors (i.e., temperature or water) are factored into the system. To fully understand the system, we need to not only continue to investigate and understand the volatile profiles but also include and understand the biochemistry of the plant's response to these stressors. In this review, we provide examples and discuss interaction considerations with respect to how readers and future authors of the Journal of Agricultural and Food Chemistry can contribute their expertise toward the extraction and interpretation of chemical information exchanged between agricultural commodities and their associated pests. This holistic, multidisciplinary, and thoughtful approach to interactions of plants, insects, and microbes, and the resultant response of the plants can lead to a better understanding of agricultural ecology, in turn leading to practical and viable solutions to agricultural problems.
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http://dx.doi.org/10.1021/acs.jafc.8b01763DOI Listing
July 2018

Contrasting insect attraction and herbivore-induced plant volatile production in maize.

Planta 2018 Jul 3;248(1):105-116. Epub 2018 Apr 3.

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

Main Conclusion: The maize inbred line W22 has lower herbivore-induced volatile production than B73 but both fall armyworm larvae and the wasps that parasitize them prefer W22 over B73. Maize inbred line W22 is an important resource for genetic studies due to the availability of the UniformMu mutant population and a complete genome sequence. In this study, we assessed the suitability of W22 as a model for tritrophic interactions between maize, Spodoptera frugiperda (fall armyworm) and the parasitoid wasp Cotesia marginiventris. W22 was found to be a good model for studying the interaction as S. frugiperda prefers W22 over B73 and a higher parasitism rate by C. marginiventris was observed on W22 compared to the inbred line B73. W22 also produced lower amounts of many herbivore-induced volatile terpenes and indole emission upon treatment with S. frugiperda oral secretions. We propose that some of the major herbivore-induced terpene volatiles are perhaps impeding S. frugiperda and C. marginiventris preference and that as yet unidentified compounds are produced at low abundance may be positively impacting these interactions.
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http://dx.doi.org/10.1007/s00425-018-2886-xDOI Listing
July 2018

MSD1 regulates pedicellate spikelet fertility in sorghum through the jasmonic acid pathway.

Nat Commun 2018 02 26;9(1):822. Epub 2018 Feb 26.

U.S. Department of Agriculture-Agricultural Research Service, Plant Stress and Germplasm Development Unit, Cropping Systems Research Laboratory, Lubbock, TX, 79415, USA.

Grain number per panicle (GNP) is a major determinant of grain yield in cereals. However, the mechanisms that regulate GNP remain unclear. To address this issue, we isolate a series of sorghum [Sorghum bicolor (L.) Moench] multiseeded (msd) mutants that can double GNP by increasing panicle size and altering floral development so that all spikelets are fertile and set grain. Through bulk segregant analysis by next-generation sequencing, we identify MSD1 as a TCP (Teosinte branched/Cycloidea/PCF) transcription factor. Whole-genome expression profiling reveals that jasmonic acid (JA) biosynthetic enzymes are transiently activated in pedicellate spikelets. Young msd1 panicles have 50% less JA than wild-type (WT) panicles, and application of exogenous JA can rescue the msd1 phenotype. Our results reveal a new mechanism for increasing GNP, with the potential to boost grain yield, and provide insight into the regulation of plant inflorescence architecture and development.
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http://dx.doi.org/10.1038/s41467-018-03238-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5826930PMC
February 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

Maize w3 disrupts homogentisate solanesyl transferase (ZmHst) and reveals a plastoquinone-9 independent path for phytoene desaturation and tocopherol accumulation in kernels.

Plant J 2018 03;93(5):799-813

University of Florida, Horticultural Sciences, 2550 Hull Rd, Gainesville, FL 32611, USA.

Maize white seedling 3 (w3) has been used to study carotenoid deficiency for almost 100 years, although the molecular basis of the mutation has remained unknown. Here we show that the w3 phenotype is caused by disruption of the maize gene for homogentisate solanesyl transferase (HST), which catalyzes the first and committed step in plastoquinone-9 (PQ-9) biosynthesis in the plastid. The resulting PQ-9 deficiency prohibits photosynthetic electron transfer and eliminates PQ-9 as an oxidant in the enzymatic desaturation of phytoene during carotenoid synthesis. As a result, light-grown w3 seedlings are albino, deficient in colored carotenoids and accumulate high levels of phytoene. However, despite the absence of PQ-9 for phytoene desaturation, dark-grown w3 seedlings can produce abscisic acid (ABA) and homozygous w3 kernels accumulate sufficient carotenoids to generate ABA needed for seed maturation. The presence of ABA and low levels of carotenoids in w3 nulls indicates that phytoene desaturase is able to use an alternate oxidant cofactor, albeit less efficiently than PQ-9. The observation that tocopherols and tocotrienols are modestly affected in w3 embryos and unaffected in w3 endosperm indicates that, unlike leaves, grain tissues deficient in PQ-9 are not subject to severe photo-oxidative stress. In addition to identifying the molecular basis for the maize w3 mutant, we: (1) show that low levels of phytoene desaturation can occur in w3 seedlings in the absence of PQ-9; and (2) demonstrate that PQ-9 and carotenoids are not required for vitamin E accumulation.
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http://dx.doi.org/10.1111/tpj.13821DOI Listing
March 2018

Herbivore-derived fatty-acid amides elicit reactive oxygen species burst in plants.

J Exp Bot 2018 02;69(5):1235-1245

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

Reactive oxygen species (ROS) can be elicited by many forms of stress, including pathogen attack, abiotic stress, damage and insect infestation. Perception of microbe- or damage-associated elicitors triggers an ROS burst in many plant species; however, the impact of herbivore fatty-acid amides on ROS elicitation remains largely unexplored. In this study we show that the lepidopteran-derived fatty-acid amide elicitor N-linolenoyl-L-glutamine (GLN18:3) can induce a ROS burst in multiple plant species. Furthermore, in Arabidopsis this ROS burst is partially dependent on the plasma membrane localized NADPH oxidases RBOHD and RBOHF, and an Arabidopsis rbohD/F double mutant produces enhanced GLN18:3-induced jasmonic acid. Quantification of GLN18:3-induced ROS in phytohormone-deficient lines revealed that in Arabidopsis reduced levels of jasmonic acid resulted in a larger elicitor-induced ROS burst, while in tomato reduction of either jasmonic acid or salicylic acid led to higher induced ROS production. These data indicate that GLN18:3-induced ROS is antagonistic to jasmonic acid production in these species. In biological assays, rbohD/F mutant plants were more resistant to the generalist herbivores Spodoptera exigua and Trichoplusia ni but not to the specialist Plutella xylostella. Collectively, these results demonstrate that in Arabidopsis herbivore-induced ROS may negatively regulate plant defense responses to herbivory.
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http://dx.doi.org/10.1093/jxb/erx449DOI Listing
February 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

RNA-Seq analysis of resistant and susceptible sub-tropical maize lines reveals a role for kauralexins in resistance to grey leaf spot disease, caused by Cercospora zeina.

BMC Plant Biol 2017 Nov 13;17(1):197. Epub 2017 Nov 13.

Department of Molecular and Cell Biology, University of Cape Town, Private Bag, Rondebosch, Cape Town, 7701, South Africa.

Background: Cercospora zeina is a foliar pathogen responsible for maize grey leaf spot in southern Africa that negatively impacts maize production. Plants use a variety of chemical and structural mechanisms to defend themselves against invading pathogens such as C. zeina, including the production of secondary metabolites with antimicrobial properties. In maize, a variety of biotic and abiotic stressors induce the accumulation of the terpenoid phytoalexins, zealexins and kauralexins.

Results: C. zeina-susceptible line displayed pervasive rectangular grey leaf spot lesions, running parallel with the leaf veins in contrast to C. zeina-resistant line that had restricted disease symptoms. Analysis of the transcriptome of both lines indicated that genes involved in primary and secondary metabolism were up-regualted, and although different pathways were prioritized in each line, production of terpenoid compounds were common to both. Targeted phytoalexin analysis revealed that C. zeina-inoculated leaves accumulated zealexins and kauralexins. The resistant line shows a propensity toward accumulation of the kauralexin B series metabolites in response to infection, which contrasts with the susceptible line that preferentially accumulates the kauralexin A series. Kauralexin accumulation was correlated to expression of the kauralexin biosynthetic gene, ZmAn2 and a candidate biosynthetic gene, ZmKSL2. We report the expression of a putative copalyl diphosphate synthase gene that is induced by C. zeina in the resistant line exclusively.

Discussion: This study shows that zealexins and kauralexins, and expression of their biosynthetic genes, are induced by C. zeina in both resistant and susceptible germplasm adapted to the southern African climate. The data presented here indicates that different forms of kauralexins accumulate in the resistant and susceptible maize lines in response to C. zeina, with the accumulation of kauralexin B compounds in a resistant maize line and kauralexin A compounds accumulating in the susceptible line.
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http://dx.doi.org/10.1186/s12870-017-1137-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5683525PMC
November 2017

Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding.

J Exp Bot 2017 07;68(16):4709-4723

Boyce Thompson Institute for Plant Research, 533 Tower Rd, Ithaca, NY 14853, USA.

Insects such as the beet armyworm (Spodoptera exigua) cause extensive damage to maize (Zea mays). Maize plants respond by triggering defense signaling, changes in gene expression, and biosynthesis of specialized metabolites. Leaves of maize inbred line B73, which has an available genome sequence, were infested with S. exigua for 1 to 24 h, followed by comparisons of the transcript and metabolite profiles with those of uninfested controls. The most extensive gene expression responses occurred rapidly, within 4-6 h after caterpillar infestation. However, both gene expression and metabolite profiles were altered within 1 h and continued to change during the entire 24 h experiment. The defensive functions of three caterpillar-induced genes were examined using available Dissociation transposon insertions in maize inbred line W22. Whereas mutations in the benzoxazinoid biosynthesis pathway (Bx1 and Bx2) significantly improved caterpillar growth, the knockout of a 13-lipoxygenase (Lox8) involved in jasmonic acid biosynthesis did not. Interestingly, 9-lipoxygenases, which lead to the production of maize death acids, were more strongly induced by caterpillar feeding than 13-lipoxygenases, suggesting an as yet unknown function in maize defense against herbivory. Together, these results provide a comprehensive view of the dynamic transcriptomic and metabolomic responses of maize leaves to caterpillar feeding.
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http://dx.doi.org/10.1093/jxb/erx274DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5853842PMC
July 2017

Elevated carbon dioxide reduces emission of herbivore-induced volatiles in Zea mays.

Plant Cell Environ 2017 Sep 23;40(9):1725-1734. Epub 2017 Jun 23.

Center for Chemical Ecology, Penn State University, University Park, PA, 16802, USA.

Terpene volatiles produced by sweet corn (Zea mays) upon infestation with pests such as beet armyworm (Spodoptera exigua) function as part of an indirect defence mechanism by attracting parasitoid wasps; yet little is known about the impact of climate change on this form of plant defence. To investigate how a central component of climate change affects indirect defence, we measured herbivore-induced volatile emissions in plants grown under elevated carbon dioxide (CO ). We found that S. exigua infested or elicitor-treated Z. mays grown at elevated CO had decreased emission of its major sesquiterpene, (E)-β-caryophyllene and two homoterpenes, (3E)-4,8-dimethyl-1,3,7-nonatriene and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene. In contrast, inside the leaves, elicitor-induced (E)-β-caryophyllene hyper-accumulated at elevated CO , while levels of homoterpenes were unaffected. Furthermore, gene expression analysis revealed that the induction of terpene synthase genes following treatment was lower in plants grown at elevated CO . Our data indicate that elevated CO leads both to a repression of volatile synthesis at the transcriptional level and to limitation of volatile release through effects of CO on stomatal conductance. These findings suggest that elevated CO may alter the ability of Z. mays to utilize volatile terpenes to mediate indirect defenses.
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http://dx.doi.org/10.1111/pce.12976DOI Listing
September 2017

Systems genetics reveals a transcriptional network associated with susceptibility in the maize-grey leaf spot pathosystem.

Plant J 2017 Feb 13;89(4):746-763. Epub 2017 Feb 13.

Department of Plant and Soil Sciences, Forestry and Agricultural Biotechnology Institute (FABI), Genomics Research Institute (GRI), University of Pretoria, Private Bag X20, Pretoria, 0028, South Africa.

We used a systems genetics approach to elucidate the molecular mechanisms of the responses of maize to grey leaf spot (GLS) disease caused by Cercospora zeina, a threat to maize production globally. Expression analysis of earleaf samples in a subtropical maize recombinant inbred line population (CML444 × SC Malawi) subjected in the field to C. zeina infection allowed detection of 20 206 expression quantitative trait loci (eQTLs). Four trans-eQTL hotspots coincided with GLS disease QTLs mapped in the same field experiment. Co-expression network analysis identified three expression modules correlated with GLS disease scores. The module (GY-s) most highly correlated with susceptibility (r = 0.71; 179 genes) was enriched for the glyoxylate pathway, lipid metabolism, diterpenoid biosynthesis and responses to pathogen molecules such as chitin. The GY-s module was enriched for genes with trans-eQTLs in hotspots on chromosomes 9 and 10, which also coincided with phenotypic QTLs for susceptibility to GLS. This transcriptional network has significant overlap with the GLS susceptibility response of maize line B73, and may reflect pathogen manipulation for nutrient acquisition and/or unsuccessful defence responses, such as kauralexin production by the diterpenoid biosynthesis pathway. The co-expression module that correlated best with resistance (TQ-r; 1498 genes) was enriched for genes with trans-eQTLs in hotspots coinciding with GLS resistance QTLs on chromosome 9. Jasmonate responses were implicated in resistance to GLS through co-expression of COI1 and enrichment of genes with the Gene Ontology term 'cullin-RING ubiquitin ligase complex' in the TQ-r module. Consistent with this, JAZ repressor expression was highly correlated with the severity of GLS disease in the GY-s susceptibility network.
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http://dx.doi.org/10.1111/tpj.13419DOI Listing
February 2017

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

Genetic mapping shows intraspecific variation and transgressive segregation for caterpillar-induced aphid resistance in maize.

Mol Ecol 2015 Nov 6;24(22):5739-50. Epub 2015 Nov 6.

Boyce Thompson Institute for Plant Research, Ithaca, NY, 14853, USA.

Plants in nature have inducible defences that sometimes lead to targeted resistance against particular herbivores, but susceptibility to others. The metabolic diversity and genetic resources available for maize (Zea mays) make this a suitable system for a mechanistic study of within-species variation in such plant-mediated interactions between herbivores. Beet armyworms (Spodoptera exigua) and corn leaf aphids (Rhopalosiphum maidis) are two naturally occurring maize herbivores with different feeding habits. Whereas chewing herbivore-induced methylation of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside (DIMBOA-Glc) to form 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA-Glc) promotes caterpillar resistance, lower DIMBOA-Glc levels favour aphid reproduction. Thus, caterpillar-induced DIMBOA-Glc methyltransferase activity in maize is predicted to promote aphid growth. To test this hypothesis, the impact of S. exigua feeding on R. maidis progeny production was assessed using seventeen genetically diverse maize inbred lines. Whereas aphid progeny production was increased by prior caterpillar feeding on lines B73, Ki11, Ki3 and Tx303, it decreased on lines Ky21, CML103, Mo18W and W22. Genetic mapping of this trait in a population of B73 × Ky21 recombinant inbred lines identified significant quantitative trait loci on maize chromosomes 1, 7 and 10. There is a transgressive segregation for aphid resistance, with the Ky21 alleles on chromosomes 1 and 7 and the B73 allele on chromosome 10 increasing aphid progeny production. The chromosome 1 QTL coincides with a cluster of three maize genes encoding benzoxazinoid O-methyltransferases that convert DIMBOA-Glc to HDMBOA-Glc. Gene expression studies and benzoxazinoid measurements indicate that S. exigua -induced responses in this pathway differentially affect R. maidis resistance in B73 and Ky21.
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http://dx.doi.org/10.1111/mec.13418DOI Listing
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

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

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