Transcriptome and quantitative proteome analysis reveals molecular processes associated with larval metamorphosis in the polychaete pseudopolydora vexillosa

Kondethimmanahalli Chandramouli; Jin Sun; FloraSy Mok; Lingli Liu; Jian-Wen Qiu; Timothy Ravasi; Pei-Yuan Qian

doi:10.1021/pr3010088

Transcriptome and quantitative proteome analysis reveals molecular processes associated with larval metamorphosis in the polychaete pseudopolydora vexillosa

Kondethimmanahalli Chandramouli, Jin Sun, FloraSy Mok, Lingli Liu, Jian-Wen Qiu, Timothy Ravasi, Pei-Yuan Qian

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

Abstract

Larval growth of the polychaete worm Pseudopolydora vexillosa involves the formation of segment-specific structures. When larvae attain competency to settle, they discard swimming chaetae and secrete mucus. The larvae build tubes around themselves and metamorphose into benthic juveniles. Understanding the molecular processes, which regulate this complex and unique transition, remains a major challenge because of the limited molecular information available. To improve this situation, we conducted high-throughput RNA sequencing and quantitative proteome analysis of the larval stages of P. vexillosa. Based on gene ontology (GO) analysis, transcripts related to cellular and metabolic processes, binding, and catalytic activities were highly represented during larval-adult transition. Mitogen-activated protein kinase (MAPK), calcium-signaling, Wnt/β-catenin, and notch signaling metabolic pathways were enriched in transcriptome data. Quantitative proteomics identified 107 differentially expressed proteins in three distinct larval stages. Fourteen and 53 proteins exhibited specific differential expression during competency and metamorphosis, respectively. Dramatic up-regulation of proteins involved in signaling, metabolism, and cytoskeleton functions were found during the larval-juvenile transition. Several proteins involved in cell signaling, cytoskeleton and metabolism were up-regulated, whereas proteins related to transcription and oxidative phosphorylation were down-regulated during competency. The integration of high-throughput RNA sequencing and quantitative proteomics allowed a global scale analysis of larval transcripts/proteins associated molecular processes in the metamorphosis of polychaete worms. Further, transcriptomic and proteomic insights provide a new direction to understand the fundamental mechanisms that regulate larval metamorphosis in polychaetes. © 2013 American Chemical Society.

Original language	English (US)
Pages (from-to)	1344-1358
Number of pages	15
Journal	Journal of Proteome Research
Volume	12
Issue number	3
DOIs	https://doi.org/10.1021/pr3010088
State	Published - Jan 29 2013

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: The authors thank Dr. Salim Bougouffa for technical help in MG-RAST data analysis, Dr. Taewoo Ryu for reviewing the transcriptome data, Ms. Cherry Kwan for proofreading the manuscript, and Dr. Wang Yong for figures preparation. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a grant from Sanya Institute of Deep-Sea Science and Engineering (SIDSSE-201206), and award SA-C0040/UK-00016 from the King Abdullah University of Science and Technology to PY Qian.

ASJC Scopus subject areas

Biochemistry
General Chemistry

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@article{0cd6f05d1fc04538ae49e14212518184,

title = "Transcriptome and quantitative proteome analysis reveals molecular processes associated with larval metamorphosis in the polychaete pseudopolydora vexillosa",

abstract = "Larval growth of the polychaete worm Pseudopolydora vexillosa involves the formation of segment-specific structures. When larvae attain competency to settle, they discard swimming chaetae and secrete mucus. The larvae build tubes around themselves and metamorphose into benthic juveniles. Understanding the molecular processes, which regulate this complex and unique transition, remains a major challenge because of the limited molecular information available. To improve this situation, we conducted high-throughput RNA sequencing and quantitative proteome analysis of the larval stages of P. vexillosa. Based on gene ontology (GO) analysis, transcripts related to cellular and metabolic processes, binding, and catalytic activities were highly represented during larval-adult transition. Mitogen-activated protein kinase (MAPK), calcium-signaling, Wnt/β-catenin, and notch signaling metabolic pathways were enriched in transcriptome data. Quantitative proteomics identified 107 differentially expressed proteins in three distinct larval stages. Fourteen and 53 proteins exhibited specific differential expression during competency and metamorphosis, respectively. Dramatic up-regulation of proteins involved in signaling, metabolism, and cytoskeleton functions were found during the larval-juvenile transition. Several proteins involved in cell signaling, cytoskeleton and metabolism were up-regulated, whereas proteins related to transcription and oxidative phosphorylation were down-regulated during competency. The integration of high-throughput RNA sequencing and quantitative proteomics allowed a global scale analysis of larval transcripts/proteins associated molecular processes in the metamorphosis of polychaete worms. Further, transcriptomic and proteomic insights provide a new direction to understand the fundamental mechanisms that regulate larval metamorphosis in polychaetes. {\textcopyright} 2013 American Chemical Society.",

author = "Kondethimmanahalli Chandramouli and Jin Sun and FloraSy Mok and Lingli Liu and Jian-Wen Qiu and Timothy Ravasi and Pei-Yuan Qian",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The authors thank Dr. Salim Bougouffa for technical help in MG-RAST data analysis, Dr. Taewoo Ryu for reviewing the transcriptome data, Ms. Cherry Kwan for proofreading the manuscript, and Dr. Wang Yong for figures preparation. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a grant from Sanya Institute of Deep-Sea Science and Engineering (SIDSSE-201206), and award SA-C0040/UK-00016 from the King Abdullah University of Science and Technology to PY Qian.",

year = "2013",

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doi = "10.1021/pr3010088",

language = "English (US)",

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T1 - Transcriptome and quantitative proteome analysis reveals molecular processes associated with larval metamorphosis in the polychaete pseudopolydora vexillosa

AU - Chandramouli, Kondethimmanahalli

AU - Sun, Jin

AU - Mok, FloraSy

AU - Liu, Lingli

AU - Qiu, Jian-Wen

AU - Ravasi, Timothy

AU - Qian, Pei-Yuan

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The authors thank Dr. Salim Bougouffa for technical help in MG-RAST data analysis, Dr. Taewoo Ryu for reviewing the transcriptome data, Ms. Cherry Kwan for proofreading the manuscript, and Dr. Wang Yong for figures preparation. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a grant from Sanya Institute of Deep-Sea Science and Engineering (SIDSSE-201206), and award SA-C0040/UK-00016 from the King Abdullah University of Science and Technology to PY Qian.

PY - 2013/1/29

Y1 - 2013/1/29

N2 - Larval growth of the polychaete worm Pseudopolydora vexillosa involves the formation of segment-specific structures. When larvae attain competency to settle, they discard swimming chaetae and secrete mucus. The larvae build tubes around themselves and metamorphose into benthic juveniles. Understanding the molecular processes, which regulate this complex and unique transition, remains a major challenge because of the limited molecular information available. To improve this situation, we conducted high-throughput RNA sequencing and quantitative proteome analysis of the larval stages of P. vexillosa. Based on gene ontology (GO) analysis, transcripts related to cellular and metabolic processes, binding, and catalytic activities were highly represented during larval-adult transition. Mitogen-activated protein kinase (MAPK), calcium-signaling, Wnt/β-catenin, and notch signaling metabolic pathways were enriched in transcriptome data. Quantitative proteomics identified 107 differentially expressed proteins in three distinct larval stages. Fourteen and 53 proteins exhibited specific differential expression during competency and metamorphosis, respectively. Dramatic up-regulation of proteins involved in signaling, metabolism, and cytoskeleton functions were found during the larval-juvenile transition. Several proteins involved in cell signaling, cytoskeleton and metabolism were up-regulated, whereas proteins related to transcription and oxidative phosphorylation were down-regulated during competency. The integration of high-throughput RNA sequencing and quantitative proteomics allowed a global scale analysis of larval transcripts/proteins associated molecular processes in the metamorphosis of polychaete worms. Further, transcriptomic and proteomic insights provide a new direction to understand the fundamental mechanisms that regulate larval metamorphosis in polychaetes. © 2013 American Chemical Society.

AB - Larval growth of the polychaete worm Pseudopolydora vexillosa involves the formation of segment-specific structures. When larvae attain competency to settle, they discard swimming chaetae and secrete mucus. The larvae build tubes around themselves and metamorphose into benthic juveniles. Understanding the molecular processes, which regulate this complex and unique transition, remains a major challenge because of the limited molecular information available. To improve this situation, we conducted high-throughput RNA sequencing and quantitative proteome analysis of the larval stages of P. vexillosa. Based on gene ontology (GO) analysis, transcripts related to cellular and metabolic processes, binding, and catalytic activities were highly represented during larval-adult transition. Mitogen-activated protein kinase (MAPK), calcium-signaling, Wnt/β-catenin, and notch signaling metabolic pathways were enriched in transcriptome data. Quantitative proteomics identified 107 differentially expressed proteins in three distinct larval stages. Fourteen and 53 proteins exhibited specific differential expression during competency and metamorphosis, respectively. Dramatic up-regulation of proteins involved in signaling, metabolism, and cytoskeleton functions were found during the larval-juvenile transition. Several proteins involved in cell signaling, cytoskeleton and metabolism were up-regulated, whereas proteins related to transcription and oxidative phosphorylation were down-regulated during competency. The integration of high-throughput RNA sequencing and quantitative proteomics allowed a global scale analysis of larval transcripts/proteins associated molecular processes in the metamorphosis of polychaete worms. Further, transcriptomic and proteomic insights provide a new direction to understand the fundamental mechanisms that regulate larval metamorphosis in polychaetes. © 2013 American Chemical Society.

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UR - https://pubs.acs.org/doi/10.1021/pr3010088

UR - http://www.scopus.com/inward/record.url?scp=84874630897&partnerID=8YFLogxK

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DO - 10.1021/pr3010088

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SN - 1535-3893

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EP - 1358

JO - Journal of Proteome Research

JF - Journal of Proteome Research

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ER -

Transcriptome and quantitative proteome analysis reveals molecular processes associated with larval metamorphosis in the polychaete pseudopolydora vexillosa

Abstract

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