Abstract
The reactive oxygen species, generally labeled toxic due to high reactivity without target specificity, are gradually uncovered as signaling molecules involved in a myriad of biological processes. But one important feature of ROS roles in macromolecule movement has not caught attention until recent studies with technique advance and design elegance have shed lights on ROS signaling for intercellular and interorganelle communication. This review begins with the discussions of genetic and chemical studies on the regulation of symplastic dye movement through intercellular tunnels in plants (plasmodesmata), and focuses on the ROS regulatory mechanisms concerning macromolecule movement including small RNA-mediated gene silencing movement and protein shuttling between cells. Given the premise that intercellular tunnels (bridges) in mammalian cells are the key physical structures to sustain intercellular communication, movement of macromolecules and signals is efficiently facilitated by ROS-induced membrane protrusions formation, which is analogously applied to the interorganelle communication in plant cells. Although ROS regulatory differences between plant and mammalian cells exist, the basis for ROS-triggered conduit formation underlies a unifying conservative theme in multicellular organisms. These mechanisms may represent the evolutionary advances that have enabled multicellularity to gain the ability to generate and utilize ROS to govern material exchanges between individual cells in oxygenated environment.
Highlights
Various cellular metabolic processes, ranging from energy capture and storage in chloroplast, long chain carbon metabolism in peroxisome, to energy generation in mitochondria, all under normal physiological condition, accompany with the generation of one type of products: the reactive oxygen species (ROS) (Halliwell and Gutteridge, 1989; Scandalios, 1997; Davies, 2000; Apel and Hirt, 2004)
The tug of war between ROS and antioxidant system has been on play since evolution of early life living in less oxic environment (Moldovan et al, 2000; Harfouche et al, 2005); for instance, the advent of enzymatic antioxidants such as superoxide dismutase (SOD), catalase and peroxiredoxin in organisms appearing on Earth around 4.1–3.5 billion years ago—around 1 billion years earlier than the great oxidation event, which highlights the paramount role of anti-ROS system in life evolution on Earth
Both ISE1 and ISE2 (INCREASED SIZE EXCLUSION LIMIT OF PLASMODESMATA 1 or 2) gene encode two different RNA helicases that are involved in the very basic aspect of RNA metabolism ranging from RNA transcription, splicing to degradation, and that are localized to mitochondria and chloroplast respectively, whereas DSE1 gene encodes a WD-repeat protein that is distributed in both cytoplasm and nucleus. These genes controlling the cell-to-cell movement of symplastic tracer appear to have no apparent intrinsic coherence in light of genetic and/or biochemical pathways or even the spacial occurrence relating to PD, TEM dissection has shown these mutants have altered architecture of PD; with increased frequency of twinned and branched PD in increased tracer movement mutant or decreased frequency of twinned and branched PD in decreased tracer movement mutant. These results have clearly shown PD-mediated transport indicated by symplastic tracer is paramount, and as such the mutants are often displaying severe phenotypic abnormalities as diverse as retarded growth, altered flowering time, dysfunctional reproductive organs, and even embryo lethal from strong mutant allele
Summary
Various cellular metabolic processes, ranging from energy capture and storage in chloroplast, long chain carbon metabolism in peroxisome, to energy generation in mitochondria, all under normal physiological condition, accompany with the generation of one type of products: the reactive oxygen species (ROS) (Halliwell and Gutteridge, 1989; Scandalios, 1997; Davies, 2000; Apel and Hirt, 2004). Rutschow et al (2011) quantified the intercellular permeability of Arabidopsis root meristematic regions by applying the diffusion model to CF bleaching experiment with confocal microscope, and generated a new measurement of PD conductivity, which is nearly an order of magnitude larger than the reported with dye microinjection (Goodwin et al, 1990) (Table 1) This value discrepancy may lie with the responsiveness of PD when subjected to the perturbation of handling or environmental stimuli, or the variation of PD components and structure in different tissues/organs (Radford and White, 2001; Roberts and Oparka, 2003). An Arg to Lys substitution in a highly conserved motif in the RCI3 peroxidase resulted in the reduced hydrogen peroxide level in the mutant
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