Comparative genomics and evidence for an unusual polyamine oxidation pathway in aquatic duckweed (Spirodela polyrhiza L.)

Polyamines (PA) cellular levels are maintained through a balance between synthesis and catabolism, achieved by two classes of enzymes polyamine oxidases (PAOs) and copper amine oxidases (CuAO). Here we investigated the occurrence, molecular evolution and role(s) of PAOs and CuAO gene families in aquatic duckweed and their comparison with other aquatic plants -sea eelgrass, bladderwort, and Lotus. We identified eight bona fide PAO genes (SpPAO1–SpPAO8) and one SpCuAO1 in the greater duckweed genome from three genome assemblies. Interestingly, duckweed PAO genes increased their number through a tandem duplication event, while contrary to this CuAO genes were significantly lost to a single gene SpCuAO1. Phylogenetic analysis revealed that tandemly duplicated SpPAO2–7 share close similarity to well-known terminal catabolism (TC) pathway PAO genes while SpPAO1 and SpPAO8 seem to segregate along with back conversion (BC) participating known PAO genes, suggesting that all tandem duplicated PAOs are involved in TC pathway which is contrary to known trend in land plants where CuAOs are mainly involved in TC pathway. Comparative transcript abundance studies indicated that all eight PAOs and one CuAO gene respond to multiple stresses and principal component analysis identifies SpPAO4 as a highly active gene in response to multiple stresses. Results showed that oxidation of higher polyamines (SPD/SPM) through the TC pathway is diversified in duckweeds. Taken together this study reveals unique insights into the genomic losses and gains of polyamine metabolism possibly involved in achieving the structural and physiological adaptations required for aquatic lifestyle of duckweeds.