Organ-specific remodeling of the Arabidopsis transcriptome in response to spaceflight

Abstract

BackgroundSpaceflight presents a novel environment that is outside the evolutionary experience of terrestrial organisms. Full activation of the International Space Station as a science platform complete with sophisticated plant growth chambers, laboratory benches, and procedures for effective sample return, has enabled a new level of research capability and hypothesis testing in this unique environment. The opportunity to examine the strategies of environmental sensing in spaceflight, which includes the absence of unit gravity, provides a unique insight into the balance of influence among abiotic cues directing plant growth and development: including gravity, light, and touch. The data presented here correlate morphological and transcriptome data from replicated spaceflight experiments.ResultsThe transcriptome of Arabidopsis thaliana demonstrated organ-specific changes in response to spaceflight, with 480 genes showing significant changes in expression in spaceflight plants compared with ground controls by at least 1.9-fold, and 58 by more than 7-fold. Leaves, hypocotyls, and roots each displayed unique patterns of response, yet many gene functions within the responses are related. Particularly represented across the dataset were genes associated with cell architecture and growth hormone signaling; processes that would not be anticipated to be altered in microgravity yet may correlate with morphological changes observed in spaceflight plants. As examples, differential expression of genes involved with touch, cell wall remodeling, root hairs, and cell expansion may correlate with spaceflight-associated root skewing, while differential expression of auxin-related and other gravity-signaling genes seemingly correlates with the microgravity of spaceflight. Although functionally related genes were differentially represented in leaves, hypocotyls, and roots, the expression of individual genes varied substantially across organ types, indicating that there is no single response to spaceflight. Rather, each organ employed its own response tactics within a shared strategy, largely involving cell wall architecture.ConclusionsSpaceflight appears to initiate cellular remodeling throughout the plant, yet specific strategies of the response are distinct among specific organs of the plant. Further, these data illustrate that in the absence of gravity plants rely on other environmental cues to initiate the morphological responses essential to successful growth and development, and that the basis for that engagement lies in the differential expression of genes in an organ-specific manner that maximizes the utilization of these signals – such as the up-regulation of genes associated with light-sensing in roots.

Seed-to-Seed-to-Seed Growth and Development of Arabidopsis in Microgravity

“…In the absence of gravity, plants rely on other environmental cues to initiate the morphological responses essential to successful growth and development through differential expression of genes in an organ-specific manner (Paul et al, 2013b). Finally, since our plants phenocopied the sgr2 and sgr3 mutants, we conclude that these mutants are good candidates for continuing to study gravity and inflorescence branching on Earth.…”

“…The majority of these plants, which underwent germination stress and delayed sprouting, were then harvested for gene expression analysis at approximately 4 weeks of age. It is therefore difficult to compare the results of our study with the recently conducted well-controlled transcriptional analysis of 12-day-old Arabidopsis plants grown on phytagel plates within the Advanced Biological Research System on a space shuttle (Paul et al, 2012(Paul et al, , 2013b.…”

Mechano-biological Coupling of Cellular Responses to Microgravity

“…Recently, the underlying mechanisms of gravisensing are elucidated intensively in plant cells by focusing on the key issues about how plant cells sense, transmit and respond to (micro-)gravity (Boonsirichai et al 2002;Blancaflor and Masson 2003;Morita 2010;Toyota and Gilrory 2013b;Sato et al 2015). Proteomic, genomic and microRNA changes are analyzed in plants or cell cultures of Arabidopsis and rice in response to gravitational alteration (i.e., microgravity, hypergravity, and clinorotation) (Barjaktarovié et al 2009;Paul et al 2013;Mazars et al 2014). Various approaches and systems are developed to quantify the mechanotransduction of plant cells (Silverberg et al 2012).…”

Flexible imaging payload for real-time fluorescent biological imaging in parabolic, suborbital and space analog environments

“…These responses can be characterized through the use of imaging hardware incorporating appropriate excitation and imaging wavelengths. The use of Green Fluorescent Protein (GFP) and its variants as biosensor molecules has served as a valuable tool in several such imaging systems (Paul et al, 2013;Stewart, 2001). Although commercial imaging systems do exist for GFP imaging, the typical configuration of these systems (e.g.…”

“…Proper imaging systems can provide real-time, macroscopic-level data on the response of biology to the spaceflight environment. These systems are also capable of delving deeper into spaceflight effects by providing information on responses at the gene expression level (Paul et al, 2013(Paul et al, , 2012. This information serves to improve our fundamental understanding of http://dx.doi.org/10.1016/j.lssr.2014.09.002 2214-5524/© 2014 The Committee on Space Research (COSPAR).…”