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The lolines are a class of bioprotective alkaloids that are produced by  Epichloë  species, fungal endophytes of grasses. These alkaloids are saturated 1-aminopyrrolizidines with a C2 to C7 ether bridge, and are structurally differentiated by the various modifications of the 1-amino group: -NH 2  (norloline), -NHCH 3  (loline), -N(CH 3 ) 2  ( N -methylloline), -N(CH 3 )Ac ( N -acetylloline), -NHAc ( N -acetylnorloline), and -N(CH 3 )CHO ( N -formylloline). Other than the LolP cytochrome P450, which is required for conversion of  N -methylloline to  N -formylloline, the enzymatic steps for loline diversification have not yet been established. Through isotopic labeling, we determined that  N -acetylnorloline is the first fully cyclized loline alkaloid, implying that deacetylation, methylation, and acetylation steps are all involved in loline alkaloid diversification. Two genes of the loline alkaloid biosynthesis ( LOL ) gene cluster,  lolN  and  lolM , were predicted to encode an  N- acetamidase (deacetylase) and a methyltransferase, respectively. A knockout strain lacking both  lolN  and  lolM  stopped the biosynthesis at  N -acetylnorloline, and complementation with the two wild-type genes restored production of  N -formylloline and  N -acetylloline. These results indicated that  lolN  and  lolM  are required in the steps from  N -acetylnorloline to other lolines. The function of LolM as an  N -methyltransferase was confirmed by its heterologous expression in yeast resulting in conversion of norloline to loline, and of loline to  N -methylloline. One of the more abundant lolines,  N -acetylloline, was observed in some but not all plants with symbiotic  Epichloë siegelii , and when provided with exogenous loline, asymbiotic meadow fescue ( Lolium pratense ) plants produced  N -acetylloline, suggesting that a plant acetyltransferase catalyzes  N -acetylloline formation. We conclude that although most loline alkaloid biosynthesis reactions are catalyzed by fungal enzymes, both fungal and plant enzymes are responsible for the chemical diversification steps  in symbio .

Enzymes from Fungal and Plant Origin Required for Chemical Diversification of Insecticidal Loline Alkaloids in Grass-Epichloë Symbiota