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

Paul AL, Zupanska AK, Schultz ER, Ferl RJ - BMC Plant Biol. (2013)

Bottom Line: The 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Horticultural Sciences, Program in Plant Molecular and Cellular Biology, University of Florida, Gainesville, FL 32611, USA.

ABSTRACT

Background: Spaceflight 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.

Results: The 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.

Conclusions: Spaceflight 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.

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Quantitative analyses across three separate spaceflight experiments. Quantitative RT-qPCR analyses were used to check the consistency of gene expression in root RNA across three separate TAGES flight experiments: Run 1B, Run 2A, and Run 2B. Runs 1B, 2A, and 2B were composed of identical Arabidopsis lines and grown under identical conditions, although in three distinct windows of time on the ISS (see Methods). The fold-change between flight and ground control is presented for five genes showing statistically significant (p < 0.01) differential expression in the microarrays conducted for the Run 2B plants (black). The RT-qPCR fold-change values (in log[2]) for each gene are presented below the array values in gradients of gray bars: Run 2B (dark gray), Run 1B (medium gray), Run 2A (light gray). Error bars for each RT-qPCR set indicate Standard Deviation with an n = 3 of biological replicates. The asterisks (***) associated with array data bars indicate p ≤0.005; otherwise, p ≤0.01. The public ID numbers for the genes presented are: DDF1 (At1g12610), DREB2A (At5g05410), TCH4 (At5g57560), JAZ7 (At2g34600), ELIP1 (At3g22840).
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Figure 4: Quantitative analyses across three separate spaceflight experiments. Quantitative RT-qPCR analyses were used to check the consistency of gene expression in root RNA across three separate TAGES flight experiments: Run 1B, Run 2A, and Run 2B. Runs 1B, 2A, and 2B were composed of identical Arabidopsis lines and grown under identical conditions, although in three distinct windows of time on the ISS (see Methods). The fold-change between flight and ground control is presented for five genes showing statistically significant (p < 0.01) differential expression in the microarrays conducted for the Run 2B plants (black). The RT-qPCR fold-change values (in log[2]) for each gene are presented below the array values in gradients of gray bars: Run 2B (dark gray), Run 1B (medium gray), Run 2A (light gray). Error bars for each RT-qPCR set indicate Standard Deviation with an n = 3 of biological replicates. The asterisks (***) associated with array data bars indicate p ≤0.005; otherwise, p ≤0.01. The public ID numbers for the genes presented are: DDF1 (At1g12610), DREB2A (At5g05410), TCH4 (At5g57560), JAZ7 (At2g34600), ELIP1 (At3g22840).

Mentions: RT-qPCR data for five selected target genes were obtained from two additional, comparable flight experiments. The genes DDF1, DREB2A, TCH4, JAZ7 and ELIP1 were initially chosen to provide quantitative support for the Run 2B array data, being selected on the basis of their high differential expression in those arrays and functional interest. This same set of genes was later used to evaluate transcriptional trends displayed by the roots of plants in the 1A and 2A flight experiments. DDF1, DREB2A, TCH4, and JAZ7 were all similarly induced in the three spaceflight growth time frames, while ELIP1 was similarly repressed (Figure 4). These data illustrated the repeatability of the spaceflight response across two separate launches and three distinct ISS growth experiments conducted months apart.


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

Paul AL, Zupanska AK, Schultz ER, Ferl RJ - BMC Plant Biol. (2013)

Quantitative analyses across three separate spaceflight experiments. Quantitative RT-qPCR analyses were used to check the consistency of gene expression in root RNA across three separate TAGES flight experiments: Run 1B, Run 2A, and Run 2B. Runs 1B, 2A, and 2B were composed of identical Arabidopsis lines and grown under identical conditions, although in three distinct windows of time on the ISS (see Methods). The fold-change between flight and ground control is presented for five genes showing statistically significant (p < 0.01) differential expression in the microarrays conducted for the Run 2B plants (black). The RT-qPCR fold-change values (in log[2]) for each gene are presented below the array values in gradients of gray bars: Run 2B (dark gray), Run 1B (medium gray), Run 2A (light gray). Error bars for each RT-qPCR set indicate Standard Deviation with an n = 3 of biological replicates. The asterisks (***) associated with array data bars indicate p ≤0.005; otherwise, p ≤0.01. The public ID numbers for the genes presented are: DDF1 (At1g12610), DREB2A (At5g05410), TCH4 (At5g57560), JAZ7 (At2g34600), ELIP1 (At3g22840).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750915&req=5

Figure 4: Quantitative analyses across three separate spaceflight experiments. Quantitative RT-qPCR analyses were used to check the consistency of gene expression in root RNA across three separate TAGES flight experiments: Run 1B, Run 2A, and Run 2B. Runs 1B, 2A, and 2B were composed of identical Arabidopsis lines and grown under identical conditions, although in three distinct windows of time on the ISS (see Methods). The fold-change between flight and ground control is presented for five genes showing statistically significant (p < 0.01) differential expression in the microarrays conducted for the Run 2B plants (black). The RT-qPCR fold-change values (in log[2]) for each gene are presented below the array values in gradients of gray bars: Run 2B (dark gray), Run 1B (medium gray), Run 2A (light gray). Error bars for each RT-qPCR set indicate Standard Deviation with an n = 3 of biological replicates. The asterisks (***) associated with array data bars indicate p ≤0.005; otherwise, p ≤0.01. The public ID numbers for the genes presented are: DDF1 (At1g12610), DREB2A (At5g05410), TCH4 (At5g57560), JAZ7 (At2g34600), ELIP1 (At3g22840).
Mentions: RT-qPCR data for five selected target genes were obtained from two additional, comparable flight experiments. The genes DDF1, DREB2A, TCH4, JAZ7 and ELIP1 were initially chosen to provide quantitative support for the Run 2B array data, being selected on the basis of their high differential expression in those arrays and functional interest. This same set of genes was later used to evaluate transcriptional trends displayed by the roots of plants in the 1A and 2A flight experiments. DDF1, DREB2A, TCH4, and JAZ7 were all similarly induced in the three spaceflight growth time frames, while ELIP1 was similarly repressed (Figure 4). These data illustrated the repeatability of the spaceflight response across two separate launches and three distinct ISS growth experiments conducted months apart.

Bottom Line: The 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Horticultural Sciences, Program in Plant Molecular and Cellular Biology, University of Florida, Gainesville, FL 32611, USA.

ABSTRACT

Background: Spaceflight 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.

Results: The 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.

Conclusions: Spaceflight 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.

Show MeSH
Related in: MedlinePlus