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

Authors: UPADHYAY, RAKESH - Purdue University; Shao, Jonathan; GRACE, ROBERTS - Volunteer; Mattoo, Autar

Submitted to: Current Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/29/2024
Publication Date: 6/3/2024
Citation: Upadhyay, R.K., Shao, J.Y., Grace, R.E., Mattoo, A.K. 2024. Comparative genomics and evidence for an unusual functional polyamine oxidation pathway in aquatic duckweed (Spirodela polyrhiza L.). Current Plant Biology. 39: Article e100359. https://doi.org/10.1016/j.cpb.2024.100359.
DOI: https://doi.org/10.1016/j.cpb.2024.100359

Interpretive Summary: Sustainable agriculture demands an understanding of key factors that also involve transition from water habitat to compact soil, particularly to understand root growth, regeneration, nutrient utilization such as nitrogen, phosphorus and potassium. These are also helpful in fulfilling our goals involving controlled environmental agriculture (CEA). We used the simplest plant, duckweed, which grows in water and provides a model to investigate fundamental questions in agricultural sustainability. The need is also for molecular framework in regard to aquatic plants versus soil plants, particularly defining the molecular evolution along with habitat change need to be identified. The molecular framework involving genes and proteins that control crucial traits in major crop plants grown in soil is therefore important. In this study, we have identified a suite of genes encoding for polyamine catabolic pathway whose product such as hydrogen peroxide serves as a signaling molecules in growth/development. Altogether, our study provides unique information about polyamines, nitrogenous amines, and polyamine oxidases in duckweed. This information is entirely different than our current knowledge obtained from soil plants. This study is important for farmers, scientists, plant physiologists, and plant genetic experts.

Technical Abstract: 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.