In recent years, we have experienced an increasing availability of -omic methods, more and more robust, for determining global changes in gene expression at the level of either gene transcription (transcriptomics), or protein mapping in quantity and quality (proteomics), or even detection of epigenetic changes (epigenomics), among others. This has made possible a substantial number of studies dealing with these kinds of changes undergone by plants when they grow in a microgravity environment, either real (spaceflight) or simulated. Transcriptomic studies, using microarray or, more recently, microsequencing (RNAseq) techniques are, by far, the most frequently performed. Some simulators are available to the local community in our lab in Madrid, while coordinating access to state of the art Ground Based Facilities at the European Space Agency (ESA) is also within our expertise.
Transcriptomic studies have produced a great deal of information on the plant responses to microgravity and spaceflight environment. The processing and interpretation of this information is, however, an arduous task, for different reasons. Spaceflight experiments are much less frequent and are subjected to much more constraints than experiments performed in ground laboratories, and this affects the reproducibility of the experiments and the statistical treatment of data. Furthermore, genotypes, growth conditions, hardware used and developmental periods of experimental samples show a great dispersion among different experiments, seriously compromising the harmonization of data. An important effort of data sharing and harmonizing has been undertaken in the project called GeneLab, under the leadership of NASA and the participation of laboratories from different countries. The project is organized into different analysis working groups (AWGs), one of them specifically devoted to plants (Barker et al. 2020; Ray et al. 2018). The European contribution to those international working groups is coordinated from our lab through the ISSOP consortium and the ESA Space Omics Topical Team.
Different genotypes, mostly from the model species Arabidopsis thaliana, and even different ecotypes of this species have been analyzed in their response to spaceflight through the Seedling Growth project in the International Space Station. No phenotypical differences were appreciated between them after growing in the space environment, but the transcriptomic results showed highly significant differences in the number and the identity of genes showing altered regulation in comparison to the respective ground controls. This would mean that each genotype, either mutant or ecotype, used a different strategy – a different set of genes – to physiologically adapt to the environmental change (Manzano et al. 2020). It is very difficult to discriminate which of the found changes are actually adaptive and which are circumstantial, unnecessary for adaptation and therefore dispensable. The definition of an affected “core set of functions”, constituted, according to available data, by the system of heat shock response genes, the oxidative stress pathways, involving the production of Reactive Oxygen Species (ROS), and the cell wall remodeling complex, though still incomplete, may help in this discrimination, but the specificities of each genotype, organ (root or aerial part) and even each cell type, in the adaptive response, should be taken into account, thus complicating the task. A subtle general stress response linked to mitochondrial function is the common response observed across both plant and animal kingdoms so far, usually observed in synergy with the adaptation to suboptimal environments as those observed in spaceflight, Moon/Mars gravity and microgravity simulation experiments (da Silveira et al. 2020; Herranz et al. 2019; Herranz et al. 2010).
Establishing cross-comparisons between the transcriptomic data from different plant spaceflight and simulation experiments is now mandatory (Gilroy et al. 2023). CSIC coordinated consortia at the European level (Deane et al. 2022; Rutter et al. 2020; Madrigal et al. 2020) are supporting GeneLab database curation of the data, providing more insight and common criteria for the exploitation and comparison of the datasets. There is also a need for the spaceflight community to be aware of the constraints of the spaceflight research, including a particular care in the preparation and analysis of ground-based reference experiments and controls (Manzano et al. 2020). Recent reviews (at The Biology of Spaceflight and Space Omics in Europe compendiums at Cell Press) present to the scientific community the current opportunities for space -omics research and discuss how to give to space biology research the opportunity to meet good practice standards similar to those of other plant biology studies. Our goal is to link our efforts with other plant biologist involved in sustainable environment goals and life support systems development.
Barker R, Lombardino J, Rasmussen K, Gilroy S (2020) Test of Arabidopsis Space Transcriptome: A Discovery Environment to Explore Multiple Plant Biology Spaceflight Experiments. Front Plant Sci 11 (147). doi:10.3389/fpls.2020.00147
da Silveira WA, Fazelinia H, Rosenthal SB, Laiakis EC, Kim MS, Meydan C, Kidane Y, Rathi KS, Smith SM, Stear B, Ying Y, Zhang Y, Foox J, Zanello S, Crucian B, Wang D, Nugent A, Costa HA, Zwart SR, Schrepfer S, Elworth RAL, Sapoval N, Treangen T, MacKay M, Gokhale NS, Horner SM, Singh LN, Wallace DC, Willey JS, Schisler JC, Meller R, McDonald JT, Fisch KM, Hardiman G, Taylor D, Mason CE, Costes SV, Beheshti A (2020) Comprehensive Multi-omics Analysis Reveals Mitochondrial Stress as a Central Biological Hub for Spaceflight Impact. Cell 183 (5):1185-1201 e1120. doi:10.1016/j.cell.2020.11.002
Deane CS, Space Omics Topical T, da Silveira WA, Herranz R (2022) Space omics research in Europe: Contributions, geographical distribution and ESA member state funding schemes. iScience 25 (3):103920. doi:10.1016/j.isci.2022.103920
Gilroy S, Barker R, Kruse CPS, Johnson C, Saravia-Butler A, Chang H-s, Trane RM, Kinscherf N, Villacampa A, Manzano A, Herranz R, Davin L, Lewis N, Perera I, Wolverton C, Gupta P, Jaiswal P, Reinsch S, Wyatt S, Fogle H (2023) Meta analysis of the space flight and microgravity response on Arabidopsis plant transcriptome. NPJ microgravity Accepted 10-January-2023:NPJMGRAV-00682R00681
Herranz R, Benguria A, Lavan DA, Lopez-Vidriero I, Gasset G, Javier Medina F, van Loon JJWA, Marco R (2010) Spaceflight-related suboptimal conditions can accentuate the altered gravity response of Drosophila transcriptome. Molecular Ecology 19 (19):4255-4264. doi:10.1111/j.1365-294X.2010.04795.x
Herranz R, Vandenbrink JP, Villacampa A, Manzano A, Poehlman WL, Feltus FA, Kiss JZ, Medina FJ (2019) RNAseq Analysis of the Response of Arabidopsis thaliana to Fractional Gravity Under Blue-Light Stimulation During Spaceflight. Frontiers in plant science 10:1529. doi:10.3389/fpls.2019.01529
Madrigal P, Gabel A, Villacampa A, Manzano A, Deane CS, Bezdan D, Carnero-Diaz E, Medina FJ, Hardiman G, Grosse I, Szewczyk N, Weging S, Giacomello S, Harridge S, Morris-Paterson T, Cahill T, Silveira WAd, Herranz R (2020) Revamping Space-omics in Europe. Cell Systems: https://doi.org/10.1016/j.cels.2020.1010.1006
Manzano A, Villacampa A, Sáez-Vasquez J, Kiss JZ, Medina FJ, Herranz R (2020) The importance of Earth reference controls in spaceflight -omics research: characterization of nucleolin mutants from the Seedling Growth experiments iScience 23 (11):101686. doi:10.1016/j.isci.2020.101686
Ray S, Gebre S, Fogle H, Berrios DC, Tran PB, Galazka JM, Costes SV (2018) GeneLab: Omics database for spaceflight experiments. Bioinformatics 35 (10):1753-1759. doi:10.1093/bioinformatics/bty884
Rutter L, Barker R, Bezdan D, Cope H, Costes SV, Degoricija L, Fisch KM, Gabitto MI, Gebre S, Giacomello S, Gilroy S, Green SJ, Mason CE, Reinsch SS, Szewczyk NJ, Taylor DM, Galazka JM, Herranz R, Muratani M (2020) A New Era for Space Life Science: International Standards for Space Omics Processing (ISSOP). Patterns:https://doi.org/10.1016/j.patter.2020.100148
(*) Open Access publications available at Cell press special Issues in 2020 https://www.cell.com/c/the-biology-of-spaceflight and 2022 https://www.sciencedirect.com/journal/iscience/special-issue/10K54CFNC0X
Space Omics Topical Team, funded by ESA (contract #4000131202/20/NL/PG/pt)
GIA2 Ground Based Facilities project, funded by ESA (contract #4000130341/20/NL/PG/pt)