Effects of Environmental Stress Factors on the Actin Cytoskeleton of Fungi and Plants: Ionizing Radiation and ROS

Abstract

Actin is an abundant and multifaceted protein in eukaryotic cells that has been detected in the cytoplasm as well as in the nucleus. In cooperation with numerous interacting accessory-proteins, monomeric actin (G-actin) polymerizes into microfilaments (F-actin) which constitute ubiquitous subcellular higher order structures. Considering the extensive spatial dimensions and multifunctionality of actin super-arrays, the present study analyses the issue if and to what extent environmental stress factors, specifically ionizing radiation (IR) and reactive oxygen species (ROS), affect the cellular actin-entity. In that context, this review particularly surveys IR-response of fungi and plants. It examines in detail which actin-related cellular constituents and molecular pathways are influenced by ionizing radiation and related ROS. This comprehensive survey concludes that the general integrity of the total cellular actin cytoskeleton is a requirement for IR-tolerance. Actin´s functions in genome organization and nuclear events like chromatin remodelling, DNA-repair, and transcription play a key role. Beyond that, it is highly significant that the macromolecular cytoplasmic and cortical actin-frameworks are affected by IR as well. In response to IR, actin-filament bundling proteins (fimbrins) are required to stabilize cables or patches. In addition, the actin-associated factors mediating cellular polarity are essential for IR-survivability. Moreover, it is concluded that a cellular homeostasis system comprising ROS, ROS-scavengers, NADPH-oxidases, and the actin cytoskeleton plays an essential role here. Consequently, besides the actin-fraction which controls crucial genome-integrity, also the portion which facilitates orderly cellular transport and polarized growth has to be maintained in order to survive IR.

Bio‐positive effects of ionizing radiation on pollen: The role of ROS

“…Unfortunately, to this day, there are still numerous open questions concerning the role of ROS in actin remodelling of plants. Specifically, the effects of IR‐associated ROS have been insufficiently investigated by only a few studies reviewed by (Stephan, 2023; Stephan, 2021). The interplay of eclectic network components which take part in the regulation of pollen tube germination and growth demonstrates itself as complex, and despite numerous studies on this subject, our picture is still fragmental.…”

“…Thus, from the entirety of all observations, the conclusion must be drawn that the action of IR on biological systems very likely depends on the distinct properties of species, individuals, tissues, cell types and their respective physiological conditions. This corresponds to a scenario which depicts IR effects as differential concerning the inherent molecular characteristics of diverse cells (Reisz et al, 2014; Stephan, 2023). In short, biochemical diversity and individual physiological status most probably represent the cause for the unequal impact of IR on various cell types.…”

“…Yet, how can this shift to higher doses be explained? Several studies demonstrate IR‐induced changes in transcription profiles in diverse plant cells (reviewed in (Stephan, 2023)), yet studies about pollen are still missing. The available data demonstrate that a substantial number of genes that are related to oxidative stress and the enzymatic antioxidant system of plant cells were particularly deregulated by IR, as well as heat shock proteins and chaperones.…”

“…The available data demonstrate that a substantial number of genes that are related to oxidative stress and the enzymatic antioxidant system of plant cells were particularly deregulated by IR, as well as heat shock proteins and chaperones. The performed microarray experiments on irradiated plants show that the number and mRNA levels of transcriptionally deregulated genes greatly vary according to irradiation conditions: acute or chronic and high or low IR doses (Gicquel et al, 2012; Kovalchuk et al, 2007; Stephan, 2023). This complicates experimentation, just as different developmental conditions or cell cycle status in plant tissues during IR exposure.…”

“…In addition, the interrelation between actin and ROS (Stephan, 2023) might play a role concerning the observed bio‐positive effects of low IR doses on pollen tube growth. The positive feedback loop between NOX(RBOH)‐produced ROS, ROS‐dependent Ca 2+ ‐channel activation, and Ca 2+ ‐dependent NOX(RBOH) activation altogether have to be fine‐tuned for orderly polarized growth (Kaya et al, 2014; Wudick and Feijo, 2014).…”