Male Fertility under Environmental Stress: Do Polyamines Act as Pollen Tube Growth Protectants?

Abstract

Although pollen structure and morphology evolved toward the optimization of stability and fertilization efficiency, its performance is affected by harsh environmental conditions, e.g., heat, cold, drought, pollutants, and other stressors. These phenomena are expected to increase in the coming years in relation to predicted environmental scenarios, contributing to a rapid increase in the interest of the scientific community in understanding the molecular and physiological responses implemented by male gametophyte to accomplish reproduction. Here, after a brief introduction summarizing the main events underlying pollen physiology with a focus on polyamine involvement in its development and germination, we review the main effects that environmental stresses can cause on pollen. We report the most relevant evidence in the literature underlying morphological, cytoskeletal, metabolic and signaling alterations involved in stress perception and response, focusing on the final stage of pollen life, i.e., from when it hydrates, to pollen tube growth and sperm cell transport, with these being the most sensitive to environmental changes. Finally, we hypothesize the molecular mechanisms through which polyamines, well-known molecules involved in plant development, stress response and adaptation, can exert a protective action against environmental stresses in pollen by decoding the essential steps and the intersection between polyamines and pollen tube growth mechanisms.

Keywords: environmental stress; plant reproduction; pollen tube growth; polyamines.

Figure 1

The main Pas identified in plant reproductive organs. Molecules were drawn using ACD/ChemSketch Freeware software (https://www.acdlabs.com/index.php, accessed on 4 January 2022).

Figure 2

Diagram illustrating some of the mechanisms regulated by PAs underlying Ca²⁺ and proton balance in pollen tube growth. It is supposed that the accumulation of both proton and Ca²⁺ ions, highlighted in the apex, depends on their influx through specific plasma membrane channels. Ion channels are under the control of other effectors; specifically, Ca²⁺ channels are regulated by receptors and small GTPases that mediate external signals. Ca²⁺ accumulation could hypothetically activate proton channels. Ca²⁺ levels are also controlled through another signaling pathway; the GTPase-receptor complex can activate the plasma membrane-associated phospholipase C (PLC) [126], which in turn generates IP3. The latter can stimulate the opening of Ca²⁺ channels. The membrane receptor system most likely also activates the production of ROS through NAD(P)H oxidase; in turn, ROS can affect Ca²⁺ flux. The action of PAs could be implemented in two distinct ways: PAs could activate the efflux of Ca²⁺ in the subapical region, while PAs could contribute to ROS production through the PAO enzyme, thus causing an increase in Ca²⁺ influx. The diagram also shows how the activation of PLC can lead to an increase in Ca²⁺ as mediated by IP₃ production. Among the membrane phospholipases, phospholipase D (PLD) [127] should also be recalled because it is responsible for the production of phosphatidic acid, a chemical mediator during stressful conditions.