Polyamine: A Potent Ameliorator for Plant Growth Response and Adaption to Abiotic Stresses Particularly the Ammonium Stress Antagonized by Urea

Abstract

Polyamine(s) (PA, PAs), a sort of N-containing and polycationic compound synthesized in almost all organisms, has been recently paid considerable attention due to its multifarious actions in the potent modulation of plant growth, development, and response to abiotic/biotic stresses. PAs in cells/tissues occur mainly in free or (non- or) conjugated forms by binding to various molecules including DNA/RNA, proteins, and (membrane-)phospholipids, thus regulating diverse molecular and cellular processes as shown mostly in animals. Although many studies have reported that an increase in internal PA may be beneficial to plant growth under abiotic conditions, leading to a suggestion of improving plant stress adaption by the elevation of endogenous PA via supply or molecular engineering of its biosynthesis, such achievements focus mainly on PA homeostasis/metabolism rather than PA-mediated molecular/cellular signaling cascades. In this study, to advance our understanding of PA biological actions important for plant stress acclimation, we gathered some significant research data to succinctly describe and discuss, in general, PA synthesis/catabolism, as well as PA as an internal ameliorator to regulate stress adaptions. Particularly, for the recently uncovered phenomenon of urea-antagonized NH₄ ⁺-stress, from a molecular and physiological perspective, we rationally proposed the possibility of the existence of PA-facilitated signal transduction pathways in plant tolerance to NH₄ ⁺-stress. This may be a more interesting issue for in-depth understanding of PA-involved growth acclimation to miscellaneous stresses in future studies.

Keywords: G-protein-coupled receptor; abiotic stress; ammonium stress; lipid signaling; polyamine and arginine; urea signal.

FIGURE 1

Schematic overview of polyamine (PA) metabolism with interconnection to other metabolic routes. Put biosynthesis may follow three pathways, of which the citrulline (Cit) pathway is reported so far only in sesame plants, where arginine (Arg) is catalyzed by Cit decarboxylase (CDC). The other two main routes include a direct conversion from ornithine (Orn) to Put by the action of ODC, and another indirect pathway with three steps, where ADC, AIH, and NCPAH sequentially decompose Arg, agmatine (Agm), and N-carbmoyl-Put, to finally generate Put. In both spermidine (Spd) and spermine (Spm) synthesize pathways, the aminopropyl moieties derived from dcSAM are required, which derived from SAM and catalyzed by the SAMDC enzyme. PA oxidases (PAOs, exhibiting apoplastic activity) catalyze an oxidation-back-reversion reaction (BC-type reaction) to generate H₂O₂ that allows “Spm to Spd and to Put” retroconversion. Another catabolite of Put is Δ¹-Pyrroline triggered by diamine oxidase (DAO). In this pathway, γ-aminobutyric acid (GABA), NO, and proline (Pro) are generated, and NO inhibits ODC activity. Regarding cellular PA-homeostasis, besides free soluble and non-covalently conjugated forms, PAs may also bind to proteins and other molecules to protect the macromolecules, regulate transporter/channel activity and gene expression, or interact with some hormones. This metabolism presentation of PAs in the plant is partially adapted from the studies by Gonzalez et al. (2021) and Spormann et al. (2021).

FIGURE 2

A proposed model of PA-participated signaling pathway in plants for urea-elicited alleviation of ammonium stress. Heterotrimeric guanine nucleotide-binding proteins (G-protein) anchor to the inner leaflet of the plasma membrane and are coupled to a putative G-protein-coupled receptor (GPCR) specific for external urea. The GPCR recognizes and binds to urea, leading to its conformation change for the activation of the G-protein(s), by which a membrane-bound adenylyl cyclase (AC) is activated to generate a second messenger cAMP. Increased cAMP activates downstream some unknown molecular component(s) to eventually modify biosynthesis pathways for PA production; the increased cAMP might also activate cAMP-dependent protein kinase to directly modulate the stress response. The subsequent activation of phospholipase C or D (PLC or PLD) by PAs promotes the generation of PIP2-derived signal molecule IP3/DAG and/or phosphatidic acid in the cytosol, resulting in the activation of an unknown inner membrane ion-channel(s) for Ca²⁺ release. An increase in cytosolic Ca²⁺ will initiate different cellular processes for specifically regulating plant growth and development under given conditions, e.g., NH₄⁺-stress with the presence of urea. This model postulated for PA-involved urea-antagonized NH₄⁺-stress is based on our recent findings (Ke et al., 2020; Liu et al., 2021) and intensive surveys of related publications cited in this study. PIP2, phosphatidylinositol 4,5-bisphosphate; IP3, inositol-triphosphate; DAG, diacylglycerol.