OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants

Vaibhav Srivastava; Ogonna Obudulu; Joakim Bygdell; Tommy Lofstedt; Patrik Ryden; Robert Nilsson; Maria Ahnlund; Annika Johansson; Par Jonsson; Eva Freyhult; Johanna Qvarnstrom; Jan Karlsson; Michael Melzer; Thomas Moritz; Johan Trygg; Torgeir R. Hvidsten; Gunnar Wingsle

doi:10.1186/1471-2164-14-893

OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants

Vaibhav Srivastava, Ogonna Obudulu, Joakim Bygdell, Tommy Lofstedt, Patrik Ryden, Robert Nilsson, Maria Ahnlund, Annika Johansson, Par Jonsson, Eva Freyhult, Johanna Qvarnstrom, Jan Karlsson, Michael Melzer, Thomas Moritz, Johan Trygg, Torgeir R. Hvidsten, Gunnar Wingsle

41 Citations (Scopus)

Abstract

Background: Reactive oxygen species (ROS) are involved in the regulation of diverse physiological processes in plants, including various biotic and abiotic stress responses. Thus, oxidative stress tolerance mechanisms in plants are complex, and diverse responses at multiple levels need to be characterized in order to understand them. Here we present system responses to oxidative stress in Populus by integrating data from analyses of the cambial region of wild-type controls and plants expressing high-isoelectric-point superoxide dismutase (hipI-SOD) transcripts in antisense orientation showing a higher production of superoxide. The cambium, a thin cell layer, generates cells that differentiate to form either phloem or xylem and is hypothesized to be a major reason for phenotypic perturbations in the transgenic plants. Data from multiple platforms including transcriptomics (microarray analysis), proteomics (UPLC/QTOF-MS), and metabolomics (GC-TOF/MS, UPLC/MS, and UHPLC-LTQ/MS) were integrated using the most recent development of orthogonal projections to latent structures called OnPLS. OnPLS is a symmetrical multi-block method that does not depend on the order of analysis when more than two blocks are analysed. Significantly affected genes, proteins and metabolites were then visualized in painted pathway diagrams. Results: The main categories that appear to be significantly influenced in the transgenic plants were pathways related to redox regulation, carbon metabolism and protein degradation, e.g. the glycolysis and pentose phosphate pathways (PPP). The results provide system-level information on ROS metabolism and responses to oxidative stress, and indicate that some initial responses to oxidative stress may share common pathways.Conclusion: The proposed data evaluation strategy shows an efficient way of compiling complex, multi-platform datasets to obtain significant biological information.

Original language	English
Journal	BMC Genomics
Volume	14
ISSN	1471-2164
DOIs	https://doi.org/10.1186/1471-2164-14-893
Publication status	Published - 17 Dec 2013
Externally published	Yes

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Srivastava, V., Obudulu, O., Bygdell, J., Lofstedt, T., Ryden, P., Nilsson, R., Ahnlund, M., Johansson, A., Jonsson, P., Freyhult, E., Qvarnstrom, J., Karlsson, J., Melzer, M., Moritz, T., Trygg, J., Hvidsten, T. R., & Wingsle, G. (2013). OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants. BMC Genomics, 14. https://doi.org/10.1186/1471-2164-14-893

OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants. / Srivastava, Vaibhav; Obudulu, Ogonna; Bygdell, Joakim et al.

In: BMC Genomics, Vol. 14, 17.12.2013.

Research output: Contribution to journal › Journal article › Research › peer-review

Srivastava, V, Obudulu, O, Bygdell, J, Lofstedt, T, Ryden, P, Nilsson, R, Ahnlund, M, Johansson, A, Jonsson, P, Freyhult, E, Qvarnstrom, J, Karlsson, J, Melzer, M, Moritz, T, Trygg, J, Hvidsten, TR & Wingsle, G 2013, 'OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants', BMC Genomics, vol. 14. https://doi.org/10.1186/1471-2164-14-893

@article{b917f22d5eb54f119a58f26c016d8972,

title = "OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants",

abstract = "Background: Reactive oxygen species (ROS) are involved in the regulation of diverse physiological processes in plants, including various biotic and abiotic stress responses. Thus, oxidative stress tolerance mechanisms in plants are complex, and diverse responses at multiple levels need to be characterized in order to understand them. Here we present system responses to oxidative stress in Populus by integrating data from analyses of the cambial region of wild-type controls and plants expressing high-isoelectric-point superoxide dismutase (hipI-SOD) transcripts in antisense orientation showing a higher production of superoxide. The cambium, a thin cell layer, generates cells that differentiate to form either phloem or xylem and is hypothesized to be a major reason for phenotypic perturbations in the transgenic plants. Data from multiple platforms including transcriptomics (microarray analysis), proteomics (UPLC/QTOF-MS), and metabolomics (GC-TOF/MS, UPLC/MS, and UHPLC-LTQ/MS) were integrated using the most recent development of orthogonal projections to latent structures called OnPLS. OnPLS is a symmetrical multi-block method that does not depend on the order of analysis when more than two blocks are analysed. Significantly affected genes, proteins and metabolites were then visualized in painted pathway diagrams. Results: The main categories that appear to be significantly influenced in the transgenic plants were pathways related to redox regulation, carbon metabolism and protein degradation, e.g. the glycolysis and pentose phosphate pathways (PPP). The results provide system-level information on ROS metabolism and responses to oxidative stress, and indicate that some initial responses to oxidative stress may share common pathways.Conclusion: The proposed data evaluation strategy shows an efficient way of compiling complex, multi-platform datasets to obtain significant biological information.",

author = "Vaibhav Srivastava and Ogonna Obudulu and Joakim Bygdell and Tommy Lofstedt and Patrik Ryden and Robert Nilsson and Maria Ahnlund and Annika Johansson and Par Jonsson and Eva Freyhult and Johanna Qvarnstrom and Jan Karlsson and Michael Melzer and Thomas Moritz and Johan Trygg and Hvidsten, {Torgeir R.} and Gunnar Wingsle",

year = "2013",

month = dec,

day = "17",

doi = "10.1186/1471-2164-14-893",

language = "English",

volume = "14",

journal = "BMC Genomics",

issn = "1471-2164",

publisher = "BioMed Central Ltd.",

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TY - JOUR

T1 - OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants

AU - Srivastava, Vaibhav

AU - Obudulu, Ogonna

AU - Bygdell, Joakim

AU - Lofstedt, Tommy

AU - Ryden, Patrik

AU - Nilsson, Robert

AU - Ahnlund, Maria

AU - Johansson, Annika

AU - Jonsson, Par

AU - Freyhult, Eva

AU - Qvarnstrom, Johanna

AU - Karlsson, Jan

AU - Melzer, Michael

AU - Moritz, Thomas

AU - Trygg, Johan

AU - Hvidsten, Torgeir R.

AU - Wingsle, Gunnar

PY - 2013/12/17

Y1 - 2013/12/17

N2 - Background: Reactive oxygen species (ROS) are involved in the regulation of diverse physiological processes in plants, including various biotic and abiotic stress responses. Thus, oxidative stress tolerance mechanisms in plants are complex, and diverse responses at multiple levels need to be characterized in order to understand them. Here we present system responses to oxidative stress in Populus by integrating data from analyses of the cambial region of wild-type controls and plants expressing high-isoelectric-point superoxide dismutase (hipI-SOD) transcripts in antisense orientation showing a higher production of superoxide. The cambium, a thin cell layer, generates cells that differentiate to form either phloem or xylem and is hypothesized to be a major reason for phenotypic perturbations in the transgenic plants. Data from multiple platforms including transcriptomics (microarray analysis), proteomics (UPLC/QTOF-MS), and metabolomics (GC-TOF/MS, UPLC/MS, and UHPLC-LTQ/MS) were integrated using the most recent development of orthogonal projections to latent structures called OnPLS. OnPLS is a symmetrical multi-block method that does not depend on the order of analysis when more than two blocks are analysed. Significantly affected genes, proteins and metabolites were then visualized in painted pathway diagrams. Results: The main categories that appear to be significantly influenced in the transgenic plants were pathways related to redox regulation, carbon metabolism and protein degradation, e.g. the glycolysis and pentose phosphate pathways (PPP). The results provide system-level information on ROS metabolism and responses to oxidative stress, and indicate that some initial responses to oxidative stress may share common pathways.Conclusion: The proposed data evaluation strategy shows an efficient way of compiling complex, multi-platform datasets to obtain significant biological information.

AB - Background: Reactive oxygen species (ROS) are involved in the regulation of diverse physiological processes in plants, including various biotic and abiotic stress responses. Thus, oxidative stress tolerance mechanisms in plants are complex, and diverse responses at multiple levels need to be characterized in order to understand them. Here we present system responses to oxidative stress in Populus by integrating data from analyses of the cambial region of wild-type controls and plants expressing high-isoelectric-point superoxide dismutase (hipI-SOD) transcripts in antisense orientation showing a higher production of superoxide. The cambium, a thin cell layer, generates cells that differentiate to form either phloem or xylem and is hypothesized to be a major reason for phenotypic perturbations in the transgenic plants. Data from multiple platforms including transcriptomics (microarray analysis), proteomics (UPLC/QTOF-MS), and metabolomics (GC-TOF/MS, UPLC/MS, and UHPLC-LTQ/MS) were integrated using the most recent development of orthogonal projections to latent structures called OnPLS. OnPLS is a symmetrical multi-block method that does not depend on the order of analysis when more than two blocks are analysed. Significantly affected genes, proteins and metabolites were then visualized in painted pathway diagrams. Results: The main categories that appear to be significantly influenced in the transgenic plants were pathways related to redox regulation, carbon metabolism and protein degradation, e.g. the glycolysis and pentose phosphate pathways (PPP). The results provide system-level information on ROS metabolism and responses to oxidative stress, and indicate that some initial responses to oxidative stress may share common pathways.Conclusion: The proposed data evaluation strategy shows an efficient way of compiling complex, multi-platform datasets to obtain significant biological information.

U2 - 10.1186/1471-2164-14-893

DO - 10.1186/1471-2164-14-893

M3 - Journal article

SN - 1471-2164

VL - 14

JO - BMC Genomics

JF - BMC Genomics

ER -

OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI- superoxide dismutase Populus plants

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