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Why Are Momilactones Always Associated with Biosynthetic Gene Clusters in Plants? COMMENTARY Juan Zhanga,B and Reuben J

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Why Are Momilactones Always Associated with Biosynthetic Gene Clusters in Plants? COMMENTARY Juan Zhanga,B and Reuben J COMMENTARY Why are momilactones always associated with biosynthetic gene clusters in plants? COMMENTARY Juan Zhanga,b and Reuben J. Petersa,1 There is an emerging realization that plant genomes intriguing hints about the distinct evolutionary pres- contain biosynthetic gene clusters (BGCs) for more sures leading to not only their assembly but also that specialized metabolism in certain cases (1). However, of BGCs in plants more generally. while horizontal gene transfer seems to drive the as- As labdane-related diterpenoids, the momilac- sembly of self-sufficient BGCs in microbes, the limita- tones require dual cyclization reactions (9). Notably, tions of strict vertical gene transmission necessitate a identification of the two relevant cyclases revealed distinct driving force for the assembly of BGCs in that the genes for these consecutively acting enzymes plants. The evidence for horizontal gene transfer of are close together in the rice genome (2). Moreover, BGCs in microbes is derived from the appearance of the only other genes in the region encode two closely homologous such loci, leading to biosynthesis of the related cytochrome P450 (CYP) monooxygenases same (or very closely related) natural products, in phy- (CYP99A2 and CYP99A3) and two short-chain alcohol logenetically distinct species. By contrast, there has dehydrogenases/reductases (SDRs) (10). The two been much less investigation of such occurrences in SDRs also are closely related, and both can catalyze plants. This is a result of many fewer examples of oxidation of the penultimate intermediate 3β-hydroxy- BGCs, as well as instances of natural products that skip syn-pimaradien-19,6β-olide to form the characteristic across phylogenetic distances in this kingdom. carbon-3 (C3) keto group of momilactone A (11). Ac- Fortunately, the momilactones provide a strikingly cordingly, these have been termed momilactone syn- informative exception. These diterpenoids were orig- thases (MS1 and MS2) (12). However, while the inally found in rice (Oryza sativa), where the associated diterpene cyclases together produce the olefin syn- BGC was among the first few identified in plants (2), pimaradiene, with CYP99A2 and CYP99A3 both func- and where they serve as allelochemicals and/or phy- tioning as subsequently acting C19 oxidases (13, 14), toalexins (3, 4). Notably, momilactones are produced the resulting syn-pimaradien-19-oic acid requires fur- by not only other wild rice species within the Oryza ther elaboration. In particular, formation of the epon- genus but also barnyard grass (Echinochloa crus-galli), ymous lactone ring clearly requires oxidation at the which falls within a separate clade of the Poaceae C6β position, while hydroxylation at C3β also is re- family. Intriguingly, beyond the expected orthologous quired. Moreover, formation of the hemiketal ring that momilactone BGCs in Oryza (5), a homologous BGC characterizes momilactone B requires hydroxylation at also was found in the phylogenetically more distant E. C20. Two other rice CYPs have been shown to react crus-galli (6). Even more interesting is the production with syn-pimaradiene at two of these positions, with of momilactones by the bryophyte Calohypnum CYP701A8 acting as a C3β-hydroxylase (14), while plumiforme (formerly Hypnum plumaeforme), repre- CYP76M8 acts as a C6β-hydroxylase (15). Yet neither senting a very early diverging lineage of land plants CYP76M8 or CYP701A8, nor any other CYP genes, are (7). In PNAS, Mao et al. (8) report that the C. plumiforme located in the rice momilactone BGC, which is then genome contains a BGC for momilactone biosynthesis. not self-sufficient (Fig. 1). Strikingly, this not only represents identification of a A somewhat similar situation is observed in the BGC in a bryophyte but, further, is clearly phylogenet- momilactone BGCs in other species from the Poa- ically distinct from the BGCs associated with momilac- ceae. Consistent with their close phylogenetic re- tone biosynthesis in the Poaceae. Nevertheless, lationship, Oryza punctata produces momilactones despite their clearly independent evolutionary origins, and contains a momilactone BGC exactly orthologous comparison of these momilactone BGCs reveals to that in O. sativa. However, only CYP99A subfamily aRoy J. Carver Department of Biochemistry, Biophysics, & Molecular Biology, Iowa State University, Ames, IA 50011; and bState Key Laboratory of Physiology and Biochemistry, College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China Author contributions: J.Z. and R.J.P. wrote the paper. The authors declare no competing interest. Published under the PNAS license. See companion article, “Genomic evidence for convergent evolution of gene clusters for momilactone biosynthesis in land plants,” 10.1073/pnas. 1914373117. 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.2007934117 PNAS Latest Articles | 1of3 Downloaded by guest on September 27, 2021 OsCPS4 CYP99A3 OsMS2 OsMS1 OsKSL4 CYP99A2 O. sativa vertical OpCPS4 CYP99A OpMS2 OpMS1 OpKSL4 CYP99A O. punctata hybridization & introgression Poaceae EcMS CYP76M EcKSL1 EcCPS1 CYP99A E. crus-galli independent evolution CpMS CYP75B CpDTC1 CYP707C tracheophytes C. plumiforme bryophytes Fig. 1. Momilactone BGC in various plants with corresponding pathway. Includes approximate phylogenetic tree for relevant plant species and corresponding momilactone BGC, with genes colored to indicate distinct enzymatic (sub)families (split coloring of CpDTC indicates bifunctional fusion of copalyl diphosphate synthase [CPS] and kaurene synthase-like [KSL] cyclases). Arrows and/or accompanying notes on the right side indicate hypothesized evolutionary relationships among the depicted momilactone BGCs. The biosynthetic pathway has been annotated to include numbering of the relevant carbons in syn-pimaradiene and the relevant enzymes from momilactone BGCs, with steps mediated by CYPs not contained within these noted, along with hypothesized phytotoxicity of certain intermediates (i.e., substrates for enzymes found within the momilactone BGCs, as discussed), in red text (CYP701A subfamily member from tandem gene array that includes the requisite ent-kaurene oxidase for gibberellin phytohormone biosynthesis). members are present in this region in the more phylogenetically The difference in composition of these momilactone BGCs distant Oryza brachyantha, with no relevant genes found at all in seems to stem from more fundamental distinctions between the even more distant Leersia perrieri, neither of which makes bryophytes and tracheophytes, in particular, the gibberellin momilactones. This indicates that such metabolism and the asso- phytohormones that are required in the latter but not the former ciated BGC arose within the Oryza lineage (5). Nevertheless, the (18). The C3β-hydroxylase for momilactone biosynthesis in the much more phylogenetically distant E. crus-galli also produces Poaceae is a member of the CYP701A subfamily, which is oth- momilactones and contains an apparently orthologous BGC. In erwise closely associated with gibberellin biosynthesis. In rice, particular, although the E. crus-galli momilactone BGC contains the relevant CYP701A8 is located in a tandem gene array that only single copies of CYP99A and MS (unlike in Oryza), and has includes the paralogous ent-kaurene oxidase required for gib- undergone some change in gene order, phylogenetic analysis of berellin phytohormone metabolism, CYP701A6,whichthenisan the genes found in both indicates nearest homology to those from essential gene (10). Moreover, such CYP701A tandem gene du- the Oryza BGC rather than with members of the relevant enzymatic plication and diversion of a paralog to more specialized metab- families from more closely related plant species (6). Interestingly, it olism (i.e., neofunctionalization) seems to be widespread in the has been hypothesized that this orthology may reflect an ancient Poaceae (19). Hence, such linkage to an essential gene removes hybridization event and subsequent natural introgression of the the need to “recruit” the C3β-hydroxylase to the momilactone momilactone BGC into the E. crus-galli lineage, which implies BGC—in particular, as coinheritance is then accomplished regard- strong selective pressure for such metabolism (16). Regardless, less. This illustrates how vertical gene transmission impacts BGC the analogous composition of all of the momilactone BGCs from assembly; that is, inheritance can be ensured even in the absence the Poaceae demonstrates that none is self-sufficient. of self-sufficient BGCs. In addition, this argues against a role for Intriguingly, the work of Mao et al. (8) reveals similar insuffi- coregulation in driving BGC assembly. ciency in the independently evolved momilactone BGC from C. By contrast, the similarities in composition, despite the plumiforme. This BGC was found by sequencing the C. plumi- incomplete natures of both independently evolved momilac- forme genome and locating the previously identified bifunctional tone BGCs, indicate that complete pathway inheritance is not diterpene cyclase CpDTC (17), revealing that the surrounding re- sufficient to explain BGC assembly in plants. Indeed, it has been gion contains two distinct CYPs, members of the CYP75B and hypothesized that such assembly requires not only positive CYP707C subfamilies, as well as an SDR. Notably, the CYP75B selection pressure provided by the bioactivity of the resulting subfamily member was shown to
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