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Comparative analysis of predicted plastid-targeted proteomes of sequenced higher plant genomes.

Schaeffer S, Harper A, Raja R, Jaiswal P, Dhingra A - PLoS ONE (2014)

Bottom Line: Two separate analyses revealed that a small subset of proteins, one representing 289 protein clusters and the other 737 unique protein sequences, are conserved between seven plastid-targeted angiosperm proteomes.Our results suggest that the current state of knowledge regarding plastid biology, preferentially based on model systems is deficient.New plant genomes are expected to enable the identification of potentially new plastid-targeted proteins that will aid in studying novel roles of plastids.

View Article: PubMed Central - PubMed

Affiliation: Department of Horticulture, Washington State University, Pullman, WA, United States of America; Molecular Plant Science Graduate Program, Washington State University, Pullman, WA, United States of America.

ABSTRACT
Plastids are actively involved in numerous plant processes critical to growth, development and adaptation. They play a primary role in photosynthesis, pigment and monoterpene synthesis, gravity sensing, starch and fatty acid synthesis, as well as oil, and protein storage. We applied two complementary methods to analyze the recently published apple genome (Malus × domestica) to identify putative plastid-targeted proteins, the first using TargetP and the second using a custom workflow utilizing a set of predictive programs. Apple shares roughly 40% of its 10,492 putative plastid-targeted proteins with that of the Arabidopsis (Arabidopsis thaliana) plastid-targeted proteome as identified by the Chloroplast 2010 project and ∼57% of its entire proteome with Arabidopsis. This suggests that the plastid-targeted proteomes between apple and Arabidopsis are different, and interestingly alludes to the presence of differential targeting of homologs between the two species. Co-expression analysis of 2,224 genes encoding putative plastid-targeted apple proteins suggests that they play a role in plant developmental and intermediary metabolism. Further, an inter-specific comparison of Arabidopsis, Prunus persica (Peach), Malus × domestica (Apple), Populus trichocarpa (Black cottonwood), Fragaria vesca (Woodland Strawberry), Solanum lycopersicum (Tomato) and Vitis vinifera (Grapevine) also identified a large number of novel species-specific plastid-targeted proteins. This analysis also revealed the presence of alternatively targeted homologs across species. Two separate analyses revealed that a small subset of proteins, one representing 289 protein clusters and the other 737 unique protein sequences, are conserved between seven plastid-targeted angiosperm proteomes. Majority of the novel proteins were annotated to play roles in stress response, transport, catabolic processes, and cellular component organization. Our results suggest that the current state of knowledge regarding plastid biology, preferentially based on model systems is deficient. New plant genomes are expected to enable the identification of potentially new plastid-targeted proteins that will aid in studying novel roles of plastids.

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Overlay of apple gene expression clusters with distinct fruit development events.Relative expression of the co-expressed genes encoding plastid-targeted proteins were merged and displayed along significant events occurring within the developmental continuum of apple fruits, adapted from Janssen et al. 2008. An additional event unique to apple fruit plastids, globule accumulation was added as described by Clijsters in 1969.
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pone-0112870-g002: Overlay of apple gene expression clusters with distinct fruit development events.Relative expression of the co-expressed genes encoding plastid-targeted proteins were merged and displayed along significant events occurring within the developmental continuum of apple fruits, adapted from Janssen et al. 2008. An additional event unique to apple fruit plastids, globule accumulation was added as described by Clijsters in 1969.

Mentions: In order to determine if genes encoding plastid-targeted proteins were indeed expressed within the fruit of apple, data from a previous study were analyzed [49]. The initial microarray experiment was a large scale analysis representing 13,000 of the ∼57,000 apple genes, and was designed around many significant physiological events occurring during apple fruit development. These 13,000 genes were compared to the genes encoding predicted plastid targeted proteins described earlier in this study. About 20% of the genes (2,224 genes) encoding predicted plastid-targeted proteins mapped back to genes represented in the Janssen study. Analysis with MultiExperiment Viewer revealed that the majority of these genes were co-expressed in 9 clusters. To show how these expression profiles may relate to important fruit developmental events, expression profiles for the co-expressed genes were overlaid with those events described in Janssen et al. (Figure 2). An additional event, plastid globule accumulation, was also added, as it was noted in developing apple fruits alongside the unstacking of photosynthetic membranes [54]. As seen in Figure 2, the gene expression of these clusters and their GO terms coincide to some extent with the processes occurring within the apple fruits. Many of the biological process GO terms and KEGG pathways associated with each gene expression cluster suggest that expression of genes encoding plastid-targeted proteins may coincide with these important events. The expression of Cluster 1 greatly mirrors the photosynthetic activity of apple fruit tissue, with highest expression occurring in young, photosynthetically-capable fruit, and expression lowering as the fruit matures and has a reduction in photosynthetic capabilities. Additionally, the expression of those genes in Cluster 2 appear to mirror the development of carotenoids, volatile compounds, and maturation of fruit, with expression lowest in young fruit and increasing as the fruit reaches maturity. In particular the expression of genes whose products are involved in lipid metabolic processes, secondary metabolic processes, biosynthetic processes, and catabolic processes, as determined via GO term enrichment would be great candidates for further study in their participation in apple fruit volatile production. Cluster 11 is particularly interesting as it is comprised of genes whose expression peaks at a single time point (60 DAA), however, the associated KEGG pathways and GO terms do not suggest a connection to the significant fruit processes of cell expansion and starch accumulation occurring at that time point. Blast2GO analysis revealed that 15.2% of the entire plastid-targeted proteome of apple lacked GO term information. However, the set of 2,224 genes represented in this study reveals that this subset is better characterized as it contains only 78 (3.5%) sequences with no associated GO terms. Of course the mere expression of a gene does not indicate that a functional protein is present within the fruit plastids as this process could be affected or controlled at a number of levels including translation, interaction with chaperone proteins, redox state of the plastid, presence of appropriate translocation proteins, protein and mRNA stability and turnover, and likely many other factors. Regardless, the data presented in this study indicate that the expression of genes encoding plastid-targeted proteins is dynamic in the fruit of Malus × domestica and may play key roles in the development and quality of apple fruit.


Comparative analysis of predicted plastid-targeted proteomes of sequenced higher plant genomes.

Schaeffer S, Harper A, Raja R, Jaiswal P, Dhingra A - PLoS ONE (2014)

Overlay of apple gene expression clusters with distinct fruit development events.Relative expression of the co-expressed genes encoding plastid-targeted proteins were merged and displayed along significant events occurring within the developmental continuum of apple fruits, adapted from Janssen et al. 2008. An additional event unique to apple fruit plastids, globule accumulation was added as described by Clijsters in 1969.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231079&req=5

pone-0112870-g002: Overlay of apple gene expression clusters with distinct fruit development events.Relative expression of the co-expressed genes encoding plastid-targeted proteins were merged and displayed along significant events occurring within the developmental continuum of apple fruits, adapted from Janssen et al. 2008. An additional event unique to apple fruit plastids, globule accumulation was added as described by Clijsters in 1969.
Mentions: In order to determine if genes encoding plastid-targeted proteins were indeed expressed within the fruit of apple, data from a previous study were analyzed [49]. The initial microarray experiment was a large scale analysis representing 13,000 of the ∼57,000 apple genes, and was designed around many significant physiological events occurring during apple fruit development. These 13,000 genes were compared to the genes encoding predicted plastid targeted proteins described earlier in this study. About 20% of the genes (2,224 genes) encoding predicted plastid-targeted proteins mapped back to genes represented in the Janssen study. Analysis with MultiExperiment Viewer revealed that the majority of these genes were co-expressed in 9 clusters. To show how these expression profiles may relate to important fruit developmental events, expression profiles for the co-expressed genes were overlaid with those events described in Janssen et al. (Figure 2). An additional event, plastid globule accumulation, was also added, as it was noted in developing apple fruits alongside the unstacking of photosynthetic membranes [54]. As seen in Figure 2, the gene expression of these clusters and their GO terms coincide to some extent with the processes occurring within the apple fruits. Many of the biological process GO terms and KEGG pathways associated with each gene expression cluster suggest that expression of genes encoding plastid-targeted proteins may coincide with these important events. The expression of Cluster 1 greatly mirrors the photosynthetic activity of apple fruit tissue, with highest expression occurring in young, photosynthetically-capable fruit, and expression lowering as the fruit matures and has a reduction in photosynthetic capabilities. Additionally, the expression of those genes in Cluster 2 appear to mirror the development of carotenoids, volatile compounds, and maturation of fruit, with expression lowest in young fruit and increasing as the fruit reaches maturity. In particular the expression of genes whose products are involved in lipid metabolic processes, secondary metabolic processes, biosynthetic processes, and catabolic processes, as determined via GO term enrichment would be great candidates for further study in their participation in apple fruit volatile production. Cluster 11 is particularly interesting as it is comprised of genes whose expression peaks at a single time point (60 DAA), however, the associated KEGG pathways and GO terms do not suggest a connection to the significant fruit processes of cell expansion and starch accumulation occurring at that time point. Blast2GO analysis revealed that 15.2% of the entire plastid-targeted proteome of apple lacked GO term information. However, the set of 2,224 genes represented in this study reveals that this subset is better characterized as it contains only 78 (3.5%) sequences with no associated GO terms. Of course the mere expression of a gene does not indicate that a functional protein is present within the fruit plastids as this process could be affected or controlled at a number of levels including translation, interaction with chaperone proteins, redox state of the plastid, presence of appropriate translocation proteins, protein and mRNA stability and turnover, and likely many other factors. Regardless, the data presented in this study indicate that the expression of genes encoding plastid-targeted proteins is dynamic in the fruit of Malus × domestica and may play key roles in the development and quality of apple fruit.

Bottom Line: Two separate analyses revealed that a small subset of proteins, one representing 289 protein clusters and the other 737 unique protein sequences, are conserved between seven plastid-targeted angiosperm proteomes.Our results suggest that the current state of knowledge regarding plastid biology, preferentially based on model systems is deficient.New plant genomes are expected to enable the identification of potentially new plastid-targeted proteins that will aid in studying novel roles of plastids.

View Article: PubMed Central - PubMed

Affiliation: Department of Horticulture, Washington State University, Pullman, WA, United States of America; Molecular Plant Science Graduate Program, Washington State University, Pullman, WA, United States of America.

ABSTRACT
Plastids are actively involved in numerous plant processes critical to growth, development and adaptation. They play a primary role in photosynthesis, pigment and monoterpene synthesis, gravity sensing, starch and fatty acid synthesis, as well as oil, and protein storage. We applied two complementary methods to analyze the recently published apple genome (Malus × domestica) to identify putative plastid-targeted proteins, the first using TargetP and the second using a custom workflow utilizing a set of predictive programs. Apple shares roughly 40% of its 10,492 putative plastid-targeted proteins with that of the Arabidopsis (Arabidopsis thaliana) plastid-targeted proteome as identified by the Chloroplast 2010 project and ∼57% of its entire proteome with Arabidopsis. This suggests that the plastid-targeted proteomes between apple and Arabidopsis are different, and interestingly alludes to the presence of differential targeting of homologs between the two species. Co-expression analysis of 2,224 genes encoding putative plastid-targeted apple proteins suggests that they play a role in plant developmental and intermediary metabolism. Further, an inter-specific comparison of Arabidopsis, Prunus persica (Peach), Malus × domestica (Apple), Populus trichocarpa (Black cottonwood), Fragaria vesca (Woodland Strawberry), Solanum lycopersicum (Tomato) and Vitis vinifera (Grapevine) also identified a large number of novel species-specific plastid-targeted proteins. This analysis also revealed the presence of alternatively targeted homologs across species. Two separate analyses revealed that a small subset of proteins, one representing 289 protein clusters and the other 737 unique protein sequences, are conserved between seven plastid-targeted angiosperm proteomes. Majority of the novel proteins were annotated to play roles in stress response, transport, catabolic processes, and cellular component organization. Our results suggest that the current state of knowledge regarding plastid biology, preferentially based on model systems is deficient. New plant genomes are expected to enable the identification of potentially new plastid-targeted proteins that will aid in studying novel roles of plastids.

Show MeSH
Related in: MedlinePlus