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

Rakesh K Upadhyay,Autar K Mattoo,Jonathan Shao

doi:10.1007/s00425-021-03755-5

Abstract

Main conclusionIdentification of the polyamine biosynthetic pathway genes in duckweed S. polyrhiza reveals presence of prokaryotic as well as land plant-type ADC pathway but absence of ODC encoding genes. Their differential gene expression and transcript abundance is shown modulated by exogenous methyl jasmonate, salinity, and acidic pH.Genetic components encoding for polyamine (PA) biosynthetic pathway are known in several land plant species; however, little is known about them in aquatic plants. We utilized recently sequenced three duckweed (Spirodela polyrhiza) genome assemblies to map PA biosynthetic pathway genes in S. polyrhiza. PA biosynthesis in most higher plants except for Arabidopsis involves two pathways, via arginine decarboxylase (ADC) and ornithine decarboxylase (ODC). ADC-mediated PA biosynthetic pathway genes, namely, 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 synthase (SpSPDS1) and one spermine synthase (SpSPMS1) in S. polyrhiza genome were identified here. However, no locus was found for ODC pathway genes in this duckweed. Hidden Markov Model protein domain analysis established that SpADC1 is a prokaryotic/biodegradative type ADC and its molecular phylogenic classification fell in a separate prokaryotic origin ADC clade with SpADC2 as a biosynthetic type of arginine decarboxylase. However, thermospermine synthase (t-SPMS)/Aculis5 genes were not found present. Instead, one of the annotated SPDS may also function as SPMS, since it was found associated with the SPMS phylogenetic clade along with known SPMS genes. Moreover, we demonstrate that S. polyrhiza PA biosynthetic gene transcripts are differentially expressed in response to unfavorable conditions, such as exogenously added salt, methyl jasmonate, or acidic pH environment as well as in extreme temperature regimes. Thus, S. polyrhiza genome encodes for complete polyamine biosynthesis pathway and the genes are transcriptionally active in response to changing environmental conditions suggesting an important role of polyamines in this aquatic plant.

Highlights

The ubiquitous polyamines (PAs) are small aliphatic biogenic amines that have been shown to impact many aspects of biological processes in many genera including plants (Kushad et al 1988; Carbonell and Navarro 1989; Flores 1991; Cohen 1998; Mehta et al 2002; Bregoli et al 2002; Kusano et al 2008; Nambeesan et al 2010, 2019; Alcázar et al 2010)
Conversion of Put to Spd is catalyzed by Spd synthase (SPDS) and, in turn, Spm/T-Spm biosynthesis of Spm and T-Spm are mediated by spermine synthase (SPMS) and thermospermine synthase (ACL5), respectively
Page 3 of 17 108 biosynthetic pathway encoding sequences for arginase/ agmatinase (ARG), arginine decarboxylase (ADC), ornithine decarboxylase (ODC), N-carbamoylputrescine amidase (CPA), agmatine iminohydroxylase (AIH) or agmatine deiminase, S-adenosylmethionine decarboxylase (SAMDc) spermidine synthase (SPDS), and spermine synthase (SPMS) from Arabidopsis (Majumdar et al 2017), tomato (Liu et al 2018; Upadhyay et al 2020b) and rice were downloaded and used as a query against S. polyrhiza genome to search for similar sequences

Summary

Introduction

The ubiquitous polyamines (PAs) are small aliphatic biogenic amines that have been shown to impact many aspects of biological processes in many genera including plants (Kushad et al 1988; Carbonell and Navarro 1989; Flores 1991; Cohen 1998; Mehta et al 2002; Bregoli et al 2002; Kusano et al 2008; Nambeesan et al 2010, 2019; Alcázar et al 2010). Works have demonstrated that PAs inhibit biosynthesis of the plant hormone ethylene in higher plants (Apelbaum et al 1981; Ben-Arie et al 1982) and shunt label from 3,4-[14C]methionine into SPD in aged orange peel discs (Even-Chen et al 1982) Their role(s) in plant development, morphogenesis, senescence, fruit set, fruit ripening, anabolic and nitrogen–carbon interactions were unearthed (Biasi et al 1988; Rastogi and Davies 1990; Shiozaki et al 2000; Mehta et al 2002; Bregoli et al 2002; Malik and Singh 2004; Tassoni et al 2004; Liu et al 2006; Ziosi et al 2006; Mattoo et al 2006; Gomez-Jimenez et al 2010; Nambeesan et al 2019).Transgenic approaches demonstrated different plant responses to diamine Put versus Spd and Spm (Mattoo et al 2010) as well as the presence of a nexus between Spm and floral organ identity and fruit set (Nambeesan et al 2019). Put catabolism is primarily mediated by diamine oxidases (CuAOs), while the terminal catabolism or back conversion of triamine SPD and tetramine SPM is modulated by polyamine oxidases (PAOs) (Cona et al 2006; Kusano et al 2008; Planas-Portell et al 2013; Kim et al 2014; Liu et al 2015)

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