Phytochemistry 172 (2020) 112289
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Phytochemistry 172 (2020) 112289 Contents lists available at ScienceDirect Phytochemistry journal homepage: www.elsevier.com/locate/phytochem Review Specialized diterpenoid metabolism in monocot crops: Biosynthesis and ☆ chemical diversity T ∗ Katherine M. Murphya, Philipp Zerbea, a Department of Plant Biology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA ARTICLE INFO ABSTRACT Keywords: Among the myriad specialized metabolites that plants employ to mediate interactions with their environment, Diterpene biosynthesis diterpenoids form a chemically diverse group with vital biological functions. A few broadly abundant diterpe- Plant specialized metabolism noids serve as core pathway intermediates in plant general metabolism. The majority of plant diterpenoids, Crop defense however, function in specialized metabolism as often species-specific chemical defenses against herbivores and Plant-environment interactions microbial diseases, in below-ground allelopathic interactions, as well as abiotic stress responses. Dynamic net- Plant natural products works of anti-microbial diterpenoids were first demonstrated in rice (Oryza sativa) over four decades ago, and more recently, unique diterpenoid blends with demonstrated antibiotic bioactivities were also discovered in maize (Zea mays). Enabled by advances in -omics and biochemical approaches, species-specific diterpenoid- diversifying enzymes have been identified in these and other Poaceous species, including wheat (Triticum aes- tivum) and switchgrass (Panicum virgatum), and are discussed in this article with an emphasis on the critical diterpene synthase and cytochrome P450 monooxygenase families and their products. The continued in- vestigation of the biosynthesis, diversity, and function of terpenoid-mediated crop defenses provides founda- tional knowledge to enable the development of strategies for improving crop resistance traits in the face of impeding pest, pathogen, and climate pressures impacting global agricultural production. 1. Introduction 2013). However, despite the extensive advances in agricultural prac- tices in the past 50 years, impeding climate shifts and associated pest Poaceous, monocot grain crops are the most important source of and disease pressures cause substantial economic losses across small- global food security. Grain consumption accounts for more than 50% of and large-scale agrosystems (Chakraborty and Newton, 2011; de Sassi world daily caloric intake, the majority of which is provided by only and Tylianakis, 2012), and threaten our ability to meet the required three crops, maize (Zea mays), wheat (Triticum aestivum), and rice agricultural outputs (Liang et al., 2017; Ray et al., 2012, 2015). In 2015 (Oryza sativa)(Food and Agriculture Organization of the United alone, fungal diseases caused a nearly 14% loss in U.S. maize produc- Nations, 2009; Tilman et al., 2011). Beyond their importance for food tion, not including harvest loss and human health risks caused by ac- and livestock feed production, monocot crops, such as maize, sorghum companying mycotoxin contamination (Crop Protection Network, (Sorghum bicolor), and switchgrass (Panicum virgatum), are of economic 2017). Similarly, insect and other herbivore damage is a major con- value as feedstock for lignocellulosic biofuel production (Mullet et al., tributor to crop losses worldwide (Oerke, 2006). At a global level, pest- 2014; Tubeileh et al., 2016). For example, 36% of maize produced in and disease-related crop losses are estimated to constitute 22–30% in the U.S. was used for ethanol production in 2016 (U.S. Department of the major cereal crops, rice, maize, and wheat, highlighting the need to Energy, 2016). develop crops that can provide nutritious food while being able to To meet the needs of a growing global population, the United withstand increasingly detrimental environmental conditions (Savary Nations has forecasted a required doubling of crop production (Food et al., 2019; Wurtzel and Kutchan, 2016). To address this challenge, and Agriculture Organization of the United Nations, 2009; Ray et al., research efforts have focused on elucidating the natural defenses Abbreviations: diTPS, diterpene synthase; GGDP, geranylgeranyl diphosphate; P450, cytochrome P450-dependent monooxygenase; CDP, copalyl diphosphate; MS, mass spectrometry; CPS, copalyl diphosphate synthase; KSL, kaurene synthase-like ☆ This invited review is associate with the award to Dr. Philipp Zerbe of the 2018 Elsevier/Phytochemical Society of North America Young Investigator Award in recognition of his outstanding contribution to studies of the biosynthesis, diversity and funcion of plant terpenoid metabolism. ∗ Corresponding author. E-mail address: [email protected] (P. Zerbe). https://doi.org/10.1016/j.phytochem.2020.112289 Received 13 December 2019; Received in revised form 24 January 2020; Accepted 28 January 2020 0031-9422/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). K.M. Murphy and P. Zerbe Phytochemistry 172 (2020) 112289 mechanisms underlying crop resilience, thus providing essential re- Unlike other terpenoids, the biosynthesis of labdane-related struc- sources for improving crop traits (Schmelz et al., 2014; Wurtzel and tures proceeds via dual biosynthetic cyclization and/or rearrangement Kutchan, 2016). reactions catalyzed by the activity of pairs of class II and class I diTPS A major mechanism by which plants interact with and adapt to their enzymes (Peters, 2010; Zerbe and Bohlmann, 2015). After initial pro- environments is through the production of elaborate cocktails of spe- tonation-initiated cyclization of GGDP into distinct bicyclic copalyl cialized metabolites. Constitutive and inducible metabolite groups ei- diphosphate (CDP) intermediates by class II diTPSs, class I diTPSs cat- ther proven or predicted to contribute to the defense against biotic and alyze the ionization of the diphosphate ester and downstream sec- abiotic stressors in monocot crops include terpenoids, phenylpropa- ondary cyclization and/or rearrangements (Peters, 2010; Karunanithi noids, oxylipins, benzoxazinoids, and carotenoids (Christensen et al., and Zerbe, 2019). Functionalization of the resulting diterpene scaffolds 2015; de Bruijn et al., 2018; Schmelz et al., 2014). Among these me- is then facilitated by P450s and select other enzyme classes such as tabolites, diterpenoids (20-carbon terpenoids) comprise a vast group of reductases, dehydrogenases, and transferases. Oxygenation reactions more than 10,000 chemically and functionally diverse natural products. catalyzed by often promiscuous P450s is essential toward forming dis- A few ubiquitously distributed diterpenoids play key roles in develop- tinct bioactive diterpenoids. Presently known P450s with functions in mental processes as intermediates of general metabolism, such as the monocot diterpenoid biosynthesis belong to the CYP71, CYP76, CYP99, biosynthesis of chlorophyll, plastoquinones, and gibberellin (GA) phy- and CYP701 families (Banerjee and Hamberger, 2018; Bathe and tohormones (Liu and Lu, 2016; Salazar-Cerezo et al., 2018). However, Tissier, 2019; Nelson and Werck-Reichhart, 2011; Schmelz et al., 2014). most diterpenoids are specialized metabolites that often represent sig- Class II and class I diTPS pairs involved in GA metabolism represent nature molecules of individual plant species or families, and biosynth- the ancestral form of these pairwise reactions and have served as a esis of which is commonly tissue- or organ-specific and underlies a strict genetic archetype to the diversification of plant specialized diterpenoid regulation by environmental stimuli (Celedon and Bohlmann, 2019; metabolism (Zi et al., 2014). Through repeated events of gene and Gershenzon and Dudareva, 2007; Schmelz et al., 2014; Tholl, 2015). genome duplication, accompanied by expansive sub- or neo-functio- Often occurring in combination with volatile mono- and sesqui-terpe- nalization, species-specific multi-enzyme diTPS and P450 families have noid defenses, higher molecular weight and typically extensively evolved (Zi et al., 2014; Bathe and Tissier, 2019; Chen et al., 2011). functionalized diterpenoids have been established as local anti- These protein families can form dynamic, modular pathway networks, microbial phytoalexins in monocot crops such as maize and rice (Block where functionally distinct and often substrate- or product-promiscuous et al., 2019; Hammerbacher et al., 2019; Peters, 2006; Schmelz et al., enzyme modules can act in different combinations to fine-tune the 2014). formation of specific diterpenoids in response to different environ- During the past decades a broader spectrum of diterpenoid functions mental stimuli (Karunanithi and Zerbe, 2019 ; Banerjee and Hamberger, has been discovered, including defenses against insect pests, bacterial 2018). Such modular pathway networks appear to be the predominant and fungal diseases, and competing weedy plants, as well as abiotic organizational structure of diterpenoid metabolism in Poaceous crops, stressors (Schmelz et al., 2014). The diversity of specialized diterpe- leading to species-specific diterpenoid blends (Schmelz et al., 2014). noids is realized by diverse families of diterpene synthase (diTPS) and Genome-wide discovery of diterpenoid pathways in rice, maize, cytochrome P450 monooxygenase (P450) enzymes that form modular wheat and switchgrass revealed diTPS families of 10–31 members