Evolutionary and functional novelty of pancreatic ribonuclease: A study of musteloidea (order Carnivora)

Jiang Liu, Xiao Ping Wang, Soochin Cho, Burton K. Lim, David M. Irwin, Oliver A. Ryder, Ya Ping Zhang, Li Yu

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Pancreatic ribonuclease (RNASE1) is a digestive enzyme that has been one of the key models in studies of evolutionary innovation and functional diversification. It has been believed that the RNASE1 gene duplications are correlated with the plant-feeding adaptation of foregut-fermenting herbivores. Here, we characterized RNASE1 genes from Caniformia, which has a simple digestive system and lacks microbial digestion typical of herbivores, in an unprecedented scope based on both gene sequence and tissue expression analyses. Remarkably, the results yielded new hypotheses regarding the evolution and the function of Caniformia RNASE1 genes. Four independent gene duplication events in the families of superfamily Musteloidea, including Procyonidae, Ailuridae, Mephitidae and Mustelidae, were recovered, rejecting previous Mustelidae-specific duplication hypothesis, but supporting Musteloidea duplication hypothesis. Moreover, our analyses revealed pronounced differences among the RNASE1 gene copies regarding their selection pressures, pI values and tissue expression patterns, suggesting the differences in their physiological functions. Notably, the expression analyses detected the transcription of a RNASE1 pseudogene in several tissues, raising the possibility that pseudogenes are also a potential source during the RNase functional diversification. In sum, the present work demonstrated a far more complex and intriguing evolutionary pattern and functional diversity of mammalian ribonuclease than previously thought.

Original languageEnglish
Article number5070
JournalScientific Reports
Volume4
DOIs
StatePublished - May 27 2014

Fingerprint

Carnivora
Pancreatic Ribonuclease
Mustelidae
Pseudogenes
Herbivory
Gene Duplication
Ribonucleases
Ailuridae
Genes
Procyonidae
Mephitidae
Digestive System
Digestion
Pressure
Enzymes

All Science Journal Classification (ASJC) codes

  • General
  • Medicine(all)

Cite this

Evolutionary and functional novelty of pancreatic ribonuclease : A study of musteloidea (order Carnivora). / Liu, Jiang; Wang, Xiao Ping; Cho, Soochin; Lim, Burton K.; Irwin, David M.; Ryder, Oliver A.; Zhang, Ya Ping; Yu, Li.

In: Scientific Reports, Vol. 4, 5070, 27.05.2014.

Research output: Contribution to journalArticle

Liu, Jiang ; Wang, Xiao Ping ; Cho, Soochin ; Lim, Burton K. ; Irwin, David M. ; Ryder, Oliver A. ; Zhang, Ya Ping ; Yu, Li. / Evolutionary and functional novelty of pancreatic ribonuclease : A study of musteloidea (order Carnivora). In: Scientific Reports. 2014 ; Vol. 4.
@article{7fd00d503a874326964931b7b23472d1,
title = "Evolutionary and functional novelty of pancreatic ribonuclease: A study of musteloidea (order Carnivora)",
abstract = "Pancreatic ribonuclease (RNASE1) is a digestive enzyme that has been one of the key models in studies of evolutionary innovation and functional diversification. It has been believed that the RNASE1 gene duplications are correlated with the plant-feeding adaptation of foregut-fermenting herbivores. Here, we characterized RNASE1 genes from Caniformia, which has a simple digestive system and lacks microbial digestion typical of herbivores, in an unprecedented scope based on both gene sequence and tissue expression analyses. Remarkably, the results yielded new hypotheses regarding the evolution and the function of Caniformia RNASE1 genes. Four independent gene duplication events in the families of superfamily Musteloidea, including Procyonidae, Ailuridae, Mephitidae and Mustelidae, were recovered, rejecting previous Mustelidae-specific duplication hypothesis, but supporting Musteloidea duplication hypothesis. Moreover, our analyses revealed pronounced differences among the RNASE1 gene copies regarding their selection pressures, pI values and tissue expression patterns, suggesting the differences in their physiological functions. Notably, the expression analyses detected the transcription of a RNASE1 pseudogene in several tissues, raising the possibility that pseudogenes are also a potential source during the RNase functional diversification. In sum, the present work demonstrated a far more complex and intriguing evolutionary pattern and functional diversity of mammalian ribonuclease than previously thought.",
author = "Jiang Liu and Wang, {Xiao Ping} and Soochin Cho and Lim, {Burton K.} and Irwin, {David M.} and Ryder, {Oliver A.} and Zhang, {Ya Ping} and Li Yu",
year = "2014",
month = "5",
day = "27",
doi = "10.1038/srep05070",
language = "English",
volume = "4",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Evolutionary and functional novelty of pancreatic ribonuclease

T2 - A study of musteloidea (order Carnivora)

AU - Liu, Jiang

AU - Wang, Xiao Ping

AU - Cho, Soochin

AU - Lim, Burton K.

AU - Irwin, David M.

AU - Ryder, Oliver A.

AU - Zhang, Ya Ping

AU - Yu, Li

PY - 2014/5/27

Y1 - 2014/5/27

N2 - Pancreatic ribonuclease (RNASE1) is a digestive enzyme that has been one of the key models in studies of evolutionary innovation and functional diversification. It has been believed that the RNASE1 gene duplications are correlated with the plant-feeding adaptation of foregut-fermenting herbivores. Here, we characterized RNASE1 genes from Caniformia, which has a simple digestive system and lacks microbial digestion typical of herbivores, in an unprecedented scope based on both gene sequence and tissue expression analyses. Remarkably, the results yielded new hypotheses regarding the evolution and the function of Caniformia RNASE1 genes. Four independent gene duplication events in the families of superfamily Musteloidea, including Procyonidae, Ailuridae, Mephitidae and Mustelidae, were recovered, rejecting previous Mustelidae-specific duplication hypothesis, but supporting Musteloidea duplication hypothesis. Moreover, our analyses revealed pronounced differences among the RNASE1 gene copies regarding their selection pressures, pI values and tissue expression patterns, suggesting the differences in their physiological functions. Notably, the expression analyses detected the transcription of a RNASE1 pseudogene in several tissues, raising the possibility that pseudogenes are also a potential source during the RNase functional diversification. In sum, the present work demonstrated a far more complex and intriguing evolutionary pattern and functional diversity of mammalian ribonuclease than previously thought.

AB - Pancreatic ribonuclease (RNASE1) is a digestive enzyme that has been one of the key models in studies of evolutionary innovation and functional diversification. It has been believed that the RNASE1 gene duplications are correlated with the plant-feeding adaptation of foregut-fermenting herbivores. Here, we characterized RNASE1 genes from Caniformia, which has a simple digestive system and lacks microbial digestion typical of herbivores, in an unprecedented scope based on both gene sequence and tissue expression analyses. Remarkably, the results yielded new hypotheses regarding the evolution and the function of Caniformia RNASE1 genes. Four independent gene duplication events in the families of superfamily Musteloidea, including Procyonidae, Ailuridae, Mephitidae and Mustelidae, were recovered, rejecting previous Mustelidae-specific duplication hypothesis, but supporting Musteloidea duplication hypothesis. Moreover, our analyses revealed pronounced differences among the RNASE1 gene copies regarding their selection pressures, pI values and tissue expression patterns, suggesting the differences in their physiological functions. Notably, the expression analyses detected the transcription of a RNASE1 pseudogene in several tissues, raising the possibility that pseudogenes are also a potential source during the RNase functional diversification. In sum, the present work demonstrated a far more complex and intriguing evolutionary pattern and functional diversity of mammalian ribonuclease than previously thought.

UR - http://www.scopus.com/inward/record.url?scp=84901499367&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84901499367&partnerID=8YFLogxK

U2 - 10.1038/srep05070

DO - 10.1038/srep05070

M3 - Article

C2 - 24861105

AN - SCOPUS:84901499367

VL - 4

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

M1 - 5070

ER -