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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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Differentially expressed genes in response to the spaceflight environment. (A) The hierarchical clustering of all 480 genes with statistically significant (p < 0.01) differential expression in the spaceflight environment by at least 1.9-fold in at least one of the three organs (LVS – Leaves; HYP – Hypocotyls; RTS – Roots). (B) A pair of Venn diagrams that illustrates the organ-specific gene expression patterns of up (red box, left) and down (green box, right) among leaves (green), hypocotyls (blue), and roots (tan). (C) A list of the 26 genes coordinately up or down regulated in all organs. The Public ID number is annotated with a brief description, and the corresponding fold-change values are shown in the columns designated for each organ. (D) A hierarchical clustering of 158 genes from (A), which have an association with cell wall remodeling and cell expansion, pathogen or wounding responses, and growth hormone signal transduction. A partial annotation of genes representative of each cluster is given to the right of the graphic. A fully annotated version of (D) is presented in Additional file3: Figure S1. Green indicates down-regulated genes and red indicates up-regulated genes. Heat-map legend values are in log[2]. Hierarchical clustering methods used on the graphics were after[20].
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Figure 3: Differentially expressed genes in response to the spaceflight environment. (A) The hierarchical clustering of all 480 genes with statistically significant (p < 0.01) differential expression in the spaceflight environment by at least 1.9-fold in at least one of the three organs (LVS – Leaves; HYP – Hypocotyls; RTS – Roots). (B) A pair of Venn diagrams that illustrates the organ-specific gene expression patterns of up (red box, left) and down (green box, right) among leaves (green), hypocotyls (blue), and roots (tan). (C) A list of the 26 genes coordinately up or down regulated in all organs. The Public ID number is annotated with a brief description, and the corresponding fold-change values are shown in the columns designated for each organ. (D) A hierarchical clustering of 158 genes from (A), which have an association with cell wall remodeling and cell expansion, pathogen or wounding responses, and growth hormone signal transduction. A partial annotation of genes representative of each cluster is given to the right of the graphic. A fully annotated version of (D) is presented in Additional file3: Figure S1. Green indicates down-regulated genes and red indicates up-regulated genes. Heat-map legend values are in log[2]. Hierarchical clustering methods used on the graphics were after[20].

Mentions: There were 480 genes that showed significant (p < 0.01) differential expression by at least 1.9-fold (Figure 3A, Additional file1) and 58 by more than 7-fold (Additional file2) in any organ; yet leaves, hypocotyls, and roots each displayed unique patterns of gene expression in response to spaceflight. Figure 3B provides a pair of Venn diagrams that illustrates the distribution patterns of differentially expressed genes among leaves (green circle), hypocotyls (blue circle), and roots (tan circle).


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

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

Differentially expressed genes in response to the spaceflight environment. (A) The hierarchical clustering of all 480 genes with statistically significant (p < 0.01) differential expression in the spaceflight environment by at least 1.9-fold in at least one of the three organs (LVS – Leaves; HYP – Hypocotyls; RTS – Roots). (B) A pair of Venn diagrams that illustrates the organ-specific gene expression patterns of up (red box, left) and down (green box, right) among leaves (green), hypocotyls (blue), and roots (tan). (C) A list of the 26 genes coordinately up or down regulated in all organs. The Public ID number is annotated with a brief description, and the corresponding fold-change values are shown in the columns designated for each organ. (D) A hierarchical clustering of 158 genes from (A), which have an association with cell wall remodeling and cell expansion, pathogen or wounding responses, and growth hormone signal transduction. A partial annotation of genes representative of each cluster is given to the right of the graphic. A fully annotated version of (D) is presented in Additional file3: Figure S1. Green indicates down-regulated genes and red indicates up-regulated genes. Heat-map legend values are in log[2]. Hierarchical clustering methods used on the graphics were after[20].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Differentially expressed genes in response to the spaceflight environment. (A) The hierarchical clustering of all 480 genes with statistically significant (p < 0.01) differential expression in the spaceflight environment by at least 1.9-fold in at least one of the three organs (LVS – Leaves; HYP – Hypocotyls; RTS – Roots). (B) A pair of Venn diagrams that illustrates the organ-specific gene expression patterns of up (red box, left) and down (green box, right) among leaves (green), hypocotyls (blue), and roots (tan). (C) A list of the 26 genes coordinately up or down regulated in all organs. The Public ID number is annotated with a brief description, and the corresponding fold-change values are shown in the columns designated for each organ. (D) A hierarchical clustering of 158 genes from (A), which have an association with cell wall remodeling and cell expansion, pathogen or wounding responses, and growth hormone signal transduction. A partial annotation of genes representative of each cluster is given to the right of the graphic. A fully annotated version of (D) is presented in Additional file3: Figure S1. Green indicates down-regulated genes and red indicates up-regulated genes. Heat-map legend values are in log[2]. Hierarchical clustering methods used on the graphics were after[20].
Mentions: There were 480 genes that showed significant (p < 0.01) differential expression by at least 1.9-fold (Figure 3A, Additional file1) and 58 by more than 7-fold (Additional file2) in any organ; yet leaves, hypocotyls, and roots each displayed unique patterns of gene expression in response to spaceflight. Figure 3B provides a pair of Venn diagrams that illustrates the distribution patterns of differentially expressed genes among leaves (green circle), hypocotyls (blue circle), and roots (tan circle).

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