Polyamines in Pollen: From Microsporogenesis to Fertilization

Abstract

The entire pollen life span is driven by polyamine (PA) homeostasis, achieved through fine regulation of their biosynthesis, oxidation, conjugation, compartmentalization, uptake, and release. The critical role of PAs, from microsporogenesis to pollen-pistil interaction during fertilization, is suggested by high and dynamic transcript levels of PA biosynthetic genes, as well as by the activities of the corresponding enzymes. Moreover, exogenous supply of PAs strongly affects pollen maturation and pollen tube elongation. A reduction of endogenous free PAs impacts pollen viability both in the early stages of pollen development and during fertilization. A number of studies have demonstrated that PAs largely function by modulating transcription, by structuring pollen cell wall, by modulating protein (mainly cytoskeletal) assembly as well as by modulating the level of reactive oxygen species. Both free low-molecular weight aliphatic PAs, and PAs conjugated to proteins and hydroxyl-cinnamic acids take part in these complex processes. Here, we review both historical and recent evidence regarding molecular events underlying the role of PAs during pollen development. In the concluding remarks, the outstanding issues and directions for future research that will further clarify our understanding of PA involvement during pollen life are outlined.

Keywords: fertilization; microsporogenesis; polyamines; putrescine; self-incompatibility; spermidine; spermine; transglutaminase.

FIGURE 1

PAs metabolism and their conjugating pathways to proteins and to hydroxyl-cinnamic acids (HCA). Free PA biosynthetic and catabolic pathways are highlighted in the yellow rectangle (A). The covalent binding to glutamyl residues of proteins gives rise to mono-γ glutamyl-PAs or to cross-links between proteins (bis-γ glutamyl-PAs) (B). The biosynthetic pathway of hydroxyl-cinnamic acids amides (HCAAs) in Arabidopsis thaliana stamens is reported according to Fellenberg et al. (2012) (C). ADC, arginine decarboxylase; ARG, arginase; AIH, agmatine iminohydrolase; CDC, citrulline decarboxylase; NCPAH, N-carbamoylputrescine amidohydrolase; ODC, ornithine decarboxylase; SAMDC, S-adenosylmethionine decarboxylase; SPDS, spermidine synthase; SPMS, spermine synthase; PAO, polyamine oxidase; SSAT, spermidine/spermine N¹-acetyltransferase; DAO, diamine oxidase; TGase, transglutaminase; SHT, Spd hydroxycinnamoyl transferase; CYP98A8/CYP98A9, P450 cytochromes; AtTMS1, Arabidopsis thaliana tapetum-specific methyltransferase, SDT, spermidine disinapoyltransferase.

FIGURE 2

Polyamines involvement during pollen development. PA biosynthetic and oxidative metabolisms occur from the early stage of pollen formation inside the anthers (A), when both microspores and the tapetal cell layer of the anther contribute to microspore cell wall architecture (B). Pollen accumulates high levels of free PAs and HCAAs, mainly localized in the cell wall. PA catabolism by PAO and DAO modulates the rigidity of the cell wall (C). Once dehydrated, pollen grains are released and PAs contribute to maintain pollen viability (D). During germination on a stigma (E), PAs promote the translation of transcripts and they are also released in the extracellular space, together with TGase (F). During pollen tube growth in a compatible style, PAs take part in the cytoskeleton organization, in cell wall deposition and remodeling by the PME enzyme as well as in the regulation of ion transport through the plasma membrane. PAs also exert an inhibitory effect on RNase enzymes (G).