Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins

Abstract

SUMMARYA 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 b-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.

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

“…ZmAN2 was first described in a differential display analysis of highly elicited transcripts following F. graminearum challenge of maize silks (Harris et al, 2005). Following the first description of ZmAN2, pathogen-elicited transcripts have been observed and reported in a large number of maize studies with diverse microbes Schmelz et al, 2011Schmelz et al, , 2014van der Linde et al, 2011;Vaughan et al, 2014;Christie et al, 2017). The nearly ubiquitous presence of ZmAN2 as a pathogen defense transcript marker is consistent with the essential biosynthetic role in the modular formation of multiple specialized diterpenoid metabolites, including not only A-and B-series kauralexins but also dolabralexins.…”

“…(+)] stereochemistry (Morrone et al, 2010). These three different combinations were selected, since ent-, syn-, and (+)-CPP represent the known stereochemical variations of class II diTPS products occurring naturally in many monocots (Peters, 2010;Schmelz et al, 2014). When coexpressed with ZmAN2, ZmKSL4 converted ent-CPP into a single product with an unusual fragmentation pattern showing major mass ions of mass-to-charge ratio (m/z) 204, 189, and 216, in addition to the mass ions m/z 257 and 272 that are characteristic of labdane diterpenoid structures (Fig.…”

“…Among these specialized metabolites, diterpenoids are a large class of more than 10,000 known compounds with diverse physiological and biological functions. Plants typically harbor both a widely conserved subset of diterpenoids such as the GAs, a class of phytohormones mediating developmental processes, and myriad specialized compounds with diverse roles in chemical ecology and plant adaptation (Keeling and Bohlmann, 2006;Gershenzon and Dudareva, 2007;Chaturvedi et al, 2012;Schmelz et al, 2014;Hedden and Sponsel, 2015). Because of their agronomic importance as two of the world's major food crops, maize (Zea mays) and rice (Oryza sativa) have been studied extensively for their terpenoid-based defense systems (Degenhardt, 2009;Schmelz et al, 2014).…”

“…Plants typically harbor both a widely conserved subset of diterpenoids such as the GAs, a class of phytohormones mediating developmental processes, and myriad specialized compounds with diverse roles in chemical ecology and plant adaptation (Keeling and Bohlmann, 2006;Gershenzon and Dudareva, 2007;Chaturvedi et al, 2012;Schmelz et al, 2014;Hedden and Sponsel, 2015). Because of their agronomic importance as two of the world's major food crops, maize (Zea mays) and rice (Oryza sativa) have been studied extensively for their terpenoid-based defense systems (Degenhardt, 2009;Schmelz et al, 2014). In rice, a suite of momilactone, oryzalexin, and phytocassane diterpenoids confer defense against several major pathogens, such as rice blast (Magnaporthe oryzae; Peters, 2006;Kato-Noguchi and Kobayashi, 2009;Toyomasu et al, 2014).…”

Probing the promiscuity of ent -kaurene oxidases via combinatorial biosynthesis

“…The difference between the activity exhibited by AtKO and OsKO2 may reflect their distinct evolutionary contexts. In particular, although Arabidopsis seems to be representative of the Brassicaceae plant family, which does not produce any more specialized LRDs, only GA, and contains just one CYP701 family member, rice is representative of the Poaceae plant family, where it has been indicated that more specialized LRDs arose early, with widespread retention (20), and rice contains a number of CYP701A subfamily members with distinct function (9)(10)(11). This presumably exerted differing selective pressures on these genes, which was examined by molecular phylogenetic analysis of all characterized members of the CYP701 family ( Fig.…”