Genomic analysis of the polyamine biosynthesis pathway in duckweed Spirodela polyrhiza L: presence of the arginine decarboxylase pathway, absence of the ornithine decarboxylase pathway, and response to abiotic stresses

Authors: UPADHYAY, RAKESH K - Purdue University; Shao, Jonathan; Mattoo, Autar

Submitted to: Planta
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/9/2021
Publication Date: 10/25/2021
Citation: Upadhyay, Rakesh K, Shao, J.Y., Mattoo, A.K. 2021. Genomic analysis of the polyamine biosynthesis pathway in duckweed Spirodela polyrhiza L.: presence of the arginine decarboxylase pathway, absence of the ornithine decarboxylase pathway, and response to abiotic stresses. Planta. 254:108. https://doi.org/10.1007/s00425-021-03755-5.
DOI: https://doi.org/10.1007/s00425-021-03755-5

Interpretive Summary: Polyamines (PAs) are important biomolecules that regulate a myriad of processes, from seed germination, plant growth, development, senescence, abiotic stress, fruit development and ripening to plant cell death. PA biosynthesis and catabolic pathways are well known in land plants. In comparison, little is known about their biosynthesis and role in aquatic plants, such as duckweed. The duckweed family has emerged as a new model system particularly because of their nutritional value. Here, we identified genetic components of the PA biosynthetic pathway in the duckweed (Spirodela polyrhiza) genome. In comparison to land plants, duckweed, like the other model plant Arabidopsis, does not have a gene for ornithine decarboxylase. We also show that duckweed possesses a prokaryotic type arginine decarboxylase sequence which possibly indicates a bacterial origin. Gene expression studies indicated that polyamine pathway genes respond to the phytohormone Methyl Jasmonate (MeJA) as well as to salt stress indicating a role in plant defense and adaptation to adverse aquatic environments. These studies advance the scientific field as a novel inclusion in databases and will help the scientific community to further understand the sustainable development of aquatic duckweed for further exploration. This research is important to scientists, biologists, geneticists, farmers, and industry.

Technical Abstract: Genetic components encoding for PA biosynthetic pathway are known in many land plant species, however, less is known about aquatic plants. We utilized three recently sequenced duckweed (Spirodela polyrhiza) genome assemblies to map polyamine (PA) biosynthetic pathway genes. PA biosynthesis in most higher plants except for Arabidopsis occurs through two pathways, involving arginine decarboxylase (ADC) and ornithine decarboxylase (ODC). Here, we present identification of the ADC-mediated PA biosynthetic pathway in the S. polyrhiza genome and note that no locus was present for ODC encoding gene(s) in this duckweed. The PA biosynthetic genes identified are one arginase (SpARG1), two arginine decarboxylases (SpADC1, SpADC2), one agmatine iminohydrolase/deiminase (SpAIH), one N-carbamoyl putrescine amidase (SpCPA), three S-adenosylmethionine decarboxylases (SpSAMDc1, 2, 3), one spermidine synthases (SpSPDS1) and one spermine synthase (SpSPMS). Hidden Markov Model (HMM) protein domain analysis established that SpADC1 is a prokaryotic/biodegradative type ADC with its molecular phylogenic classification falling in a separate prokaryotic origin ADC clade while SpADC2 is a biosynthetic type of arginine decarboxylase. No gene encoding for Thermospermine Synthase (t-SPMS)/Aculis5) was found. Also, the phylogenetic analysis indicated that one of the annotated SPDS2 may also function as SPMS since it was found associated with SPMS phylogenetic clade along with known SPMS genes. In comparison to Arabidopsis, tomato, and rice the total number of PA biosynthetic pathway genes actually decreased in S. polyrhiza. Transcript abundance analysis of genes encoding for PA pathway enzymes in two duckweed clones 7498 and 7003 showed their differential expression. Further, S. polyrhiza PA biosynthetic gene transcripts were found differentially regulated in response to exogenous salt or methyl jasmonate. The acidic pH of 1.0 induces PA pathway genes to high levels suggesting that duckweed survival at low pH is maneuvered by PAs. This novel report maps the polyamine biosynthetic pathway genes in duckweed.