plants Review Synthesis and Functions of Jasmonates in Maize Eli J. Borrego and Michael V. Kolomiets * Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA; [email protected] * Correspondence: [email protected]; Tel.: +1-979-458-4624 Academic Editor: Eve Syrkin Wurtele Received: 29 October 2016; Accepted: 22 November 2016; Published: 29 November 2016 Abstract: Of the over 600 oxylipins present in all plants, the phytohormone jasmonic acid (JA) remains the best understood in terms of its biosynthesis, function and signaling. Much like their eicosanoid analogues in mammalian system, evidence is growing for the role of the other oxylipins in diverse physiological processes. JA serves as the model plant oxylipin species and regulates defense and development. For several decades, the biology of JA has been characterized in a few dicot species, yet the function of JA in monocots has only recently begun to be elucidated. In this work, the synthesis and function of JA in maize is presented from the perspective of oxylipin biology. The maize genes responsible for catalyzing the reactions in the JA biosynthesis are clarified and described. Recent studies into the function of JA in maize defense against insect herbivory, pathogens and its role in growth and development are highlighted. Additionally, a list of JA-responsive genes is presented for use as biological markers for improving future investigations into JA signaling in maize. Keywords: jasmonic acid; maize; lipoxygenase; oxylipins; plant-insect interactions; plant-microbe interactions 1. Importance of Maize as a Crop and a Genetic Model Despite contributing over 50% of the annual calories for humans [1] and 34% of the production for animal feed [2], little is known about fundamental hormone biology in monocot plants compared to greater advances with dicot plants, primarily Arabidopsis. Maize is a diploid large grain cereal possessing unique reproductive organs where the male and female sexual organs are spatially separated. It also has a rich cultural heritage. Of all of the top most cultivated monocot crops, maize (Zea mays L.) is the only one with New World origins. Several characteristics of maize facilitate its use as a model organism to explore fundamental processes: the maize genome was recently sequenced for the B73 [3] and Palomero Toluqueño [4] lines; its separated sexual organs allow for effortless controlled pollination; it possesses tremendous genetic diversity; and it is backed by an intensely collaborative scientific community [5]. Maize and its closest crop relative, Sorghum bicolor, belong to the Panicoideae subfamily of the grasses [6] and utilize C4 carbon metabolism, an adaptation to high light intensities, temperatures and low water availability [7]. In contrast, most other economically-important cereals, such as wheat, rice and barley, belong to the Pooideae subfamily and utilize the more common C3 carbon metabolism. In recent years, scientific communities have sought to establish Brachypodium distachyon [8] and Setaria viridis [9] as monocot models for the Pooideae and Panicoideae, respectively [10]. Modern maize arose from an ancient hybridization event between two closely related diploid species that resulted in doubling of the genome (i.e., allopolyploidization) between 8.5 and 13 million years ago [11]. Eventually, the genome of this ancestor was reduced to the diploid state, but with uneven gene loss [3]. This resulted in many maize genes, including jasmonic acid (JA) biosynthesis genes, occurring as pairs throughout the genome. Plants 2016, 5, 41; doi:10.3390/plants5040041 www.mdpi.com/journal/plants Plants 2016, 5, 41 2 of 24 diploid state, but with uneven gene loss [3]. This resulted in many maize genes, including jasmonic Plantsacid (JA)2016, biosynthesis5, 41 genes, occurring as pairs throughout the genome. 2 of 25 2. Jasmonates Belong to Oxylipins, a Group of Signals Better Understood in Mammals 2. Jasmonates Belong to Oxylipins, a Group of Signals Better Understood in Mammals JAs belong to the immense group of oxygenated fatty acid products known collectively as oxylipins.JAs belong Oxylipins to the immenseare derived group from of oxygenated either enzymatic fatty acid productsor autoxidation known collectivelyof free asor oxylipins.membrane-esterified Oxylipins are fatty derived acids. from Since either all enzymaticmetabolic orprocesses autoxidation in cells of free are orenclosed membrane-esterified within fatty fattyacid-containing acids. Since allmembranes, metabolic processesoxylipins inare cells univer are enclosedsally produced within fatty across acid-containing all kingdoms membranes, of life. oxylipinsUndeniably, are oxylipins universally are produced best understood across all in kingdoms mammals of and life. in Undeniably, these organisms oxylipins are aretermed best understoodeicosanoids. inEicosanoids mammals are and furt in theseher categorized organisms into are termedsubgroups eicosanoids. based on their Eicosanoids chemical are structure further categorizedand the enzymes into subgroups(e.g., lipoxygenases, based on theircyclooxygenases chemical structure and epoxygenases) and the enzymes that catalyze (e.g., lipoxygenases, the fatty acid cyclooxygenasesoxygenation. The andmajor epoxygenases) subgroup of thatenzymaticall catalyzey-derived the fatty acidmammalian oxygenation. oxylipins The are major leukotrienes, subgroup ofprostaglandins, enzymatically-derived prostacyclins, mammalian thromboxanes, oxylipins lip areoxins, leukotrienes, eoxins, hydroxyeicosatetraenoic prostaglandins, prostacyclins, acids thromboxanes,(HETEs) and epoxyeicosatrienoic lipoxins, eoxins, hydroxyeicosatetraenoic acids (EETs), while chemically-pro acids (HETEs)duced and eicosanoids epoxyeicosatrienoic are known acids as (EETs),isoprostanes while chemically-produced[12]. In mammals, eicosanoidsoxylipins areregulate known diverse as isoprostanes physiological [12]. In processes, mammals, oxylipinssuch as regulatevasoconstriction, diverse physiologicalvasodilation, processes,pain response such asan vasoconstriction,d fever generation. vasodilation, A central pain characteristic response and of fevereicosanoid generation. activity A centralis their characteristic cell-type-dependent of eicosanoid responses, activity which is their occur cell-type-dependent from the receptor-ligand responses, whichbinding occur of specific from the eicosanoid receptor-ligand with bindingits particular of specific receptor eicosanoid [13]. In with addition its particular to receptor-ligand receptor [13]. Insignaling, addition oxylipins to receptor-ligand also possess signaling, direct antimicrobial oxylipins also activity possess [14] direct and antimicrobialare capable of activityaltering [ 14cellular] and areredox capable status of [15]. altering cellular redox status [15]. Eicosanoids were were first first identified identified in 1935 in with1935 thewith discovery the discovery of prostaglandins of prostaglandins in seminal fluidin seminal [16,17]; however,fluid [16,17]; significant however, strides significant in eicosanoid strides function in ei didcosanoid not occur function until after did the not development occur until of syntheticafter the eicosanoiddevelopment standards of synthetic and improved eicosanoid analytical standards techniques. and improved Figure1 representsanalytical thetechniques. number ofFigure articles 1 publishedrepresents each the number year from of 1949articles through published 2015 aseach indexed year from by ISI 1949 Web through of Science 201 using5 as indexed eicosanoids by ISI (terms Web used:of Science “prostaglandin”, using eicosanoids “thromboxane” (terms used: and “prostaglandin”, “leukotrienes”), jasmonates“thromboxane” (terms and used: “leukotrienes”), “jasmonate”, “jasmonic”,jasmonates “jasmonyl”(terms used: and “jasmonate”, “jasmone” [18 “jasmonic”,]) and plant oxylipins“jasmonyl” (term and used: “jasmone” “oxylipins”) [18]) andand related plant oxylipinoxylipins terms. (term The used: first “oxylipins”) dramatic increase and related in the number oxylipin of articlesterms. publishedThe first dramatic with the termsincrease associated in the withnumber eicosanoids of articles in thepublished early 1970s with corresponds the terms toassociated the development with eicosanoids of methods in of the the synthesisearly 1970s of prostaglandinscorresponds to [19the]. Anotherdevelopment substantial of methods increase of in the the earlysynthesis 1990s of coincides prostaglandins with the [19]. development Another ofsubstantial electrospray increase ionization, in the early an essential 1990s coincides component with for the the development detection of of biomolecules electrospray throughionization, mass an spectrometryessential component [20]. for the detection of biomolecules through mass spectrometry [20]. Articles published each year for the given topic terms 6000 prostaglandin, thromboxane, leukotriene jasmonate, jasmonic, jasmonyl, jasmone 5000 oxylipins 4000 3000 2000 Number of Articles ofNumber 1000 0 Year: 1949 1960 1964 1967 1970 1973 1976 1979 1982 1985 1988 1991 1994 1997 2000 2003 2006 2009 2012 2015 Figure 1.1. Articles published each year for the givengiven topic terms related to mammalianmammalian and plant oxylipins.oxylipins. The x-axis represents year from 1949 to 2015 andand y-axis represents the numbernumber of articlesarticles published eacheach year year for for the the selected selected topic topic terms. term Thes. line The representing line representing the