Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

Kenji Fukushima; Xiaodong Fang; David Alvarez-Ponce; Huimin Cai; Lorenzo Carretero-Paulet; Cui Chen; Tien Hao Chang; Kimberly M. Farr; Tomomichi Fujita; Yuji Hiwatashi; Yoshikazu Hoshi; Takamasa Imai; Masahiro Kasahara; Pablo Librado; Likai Mao; Hitoshi Mori; Tomoaki Nishiyama; Masafumi Nozawa; Gergo Pálfalvi; Stephen T. Pollard; Julio Rozas; Alejandro Sánchez-Gracia; David Sankoff; Tomoko F. Shibata; Shuji Shigenobu; Naomi Sumikawa; Taketoshi Uzawa; Meiying Xie; Chunfang Zheng; David D. Pollock; Victor A. Albert; Shuaicheng Li; Mitsuyasu Hasebe

doi:10.1038/s41559-016-0059

Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

Kenji Fukushima
, Xiaodong Fang
, David Alvarez-Ponce
, Huimin Cai
, Lorenzo Carretero-Paulet
, Cui Chen
, Tien Hao Chang
, Kimberly M. Farr
, Tomomichi Fujita
, Yuji Hiwatashi
, Yoshikazu Hoshi
, Takamasa Imai
, Masahiro Kasahara
, Pablo Librado
, Likai Mao
, Hitoshi Mori
, Tomoaki Nishiyama
, Masafumi Nozawa
, Gergo Pálfalvi
, Stephen T. Pollard

Julio Rozas, Alejandro Sánchez-Gracia, David Sankoff, Tomoko F. Shibata, Shuji Shigenobu, Naomi Sumikawa, Taketoshi Uzawa, Meiying Xie, Chunfang Zheng, David D. Pollock, Victor A. Albert, Shuaicheng Li, Mitsuyasu Hasebe

Biological Sciences

National Institute for Basic Biology
The Graduate University for Advanced Studies
University of Colorado Anschutz Medical Campus
BGI-Shenzhen
City University of Hong Kong
University of Nevada, Reno
Ghent University
SUNY Buffalo
Hokkaido University
Miyagi University
Tokai University
The University of Tokyo
University of Barcelona
University of Copenhagen
Nagoya University
Kanazawa University
Tokyo Metropolitan University
University of Ottawa
Tohoku University
Osaka Kyoiku University

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

114 Scopus citations

Abstract

Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.

Original language	English
Article number	0059
Journal	Nature Ecology and Evolution
Volume	1
Issue number	3
DOIs	https://doi.org/10.1038/s41559-016-0059
State	Published - Feb 6 2017

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Fukushima, K., Fang, X., Alvarez-Ponce, D., Cai, H., Carretero-Paulet, L., Chen, C., Chang, T. H., Farr, K. M., Fujita, T., Hiwatashi, Y., Hoshi, Y., Imai, T., Kasahara, M., Librado, P., Mao, L., Mori, H., Nishiyama, T., Nozawa, M., Pálfalvi, G., ... Hasebe, M. (2017). Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nature Ecology and Evolution, 1(3), Article 0059. https://doi.org/10.1038/s41559-016-0059

@article{f5d43f48268640a0b328da27875e279a,

title = "Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory",

abstract = "Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.",

author = "Kenji Fukushima and Xiaodong Fang and David Alvarez-Ponce and Huimin Cai and Lorenzo Carretero-Paulet and Cui Chen and Chang, \{Tien Hao\} and Farr, \{Kimberly M.\} and Tomomichi Fujita and Yuji Hiwatashi and Yoshikazu Hoshi and Takamasa Imai and Masahiro Kasahara and Pablo Librado and Likai Mao and Hitoshi Mori and Tomoaki Nishiyama and Masafumi Nozawa and Gergo P{\'a}lfalvi and Pollard, \{Stephen T.\} and Julio Rozas and Alejandro S{\'a}nchez-Gracia and David Sankoff and Shibata, \{Tomoko F.\} and Shuji Shigenobu and Naomi Sumikawa and Taketoshi Uzawa and Meiying Xie and Chunfang Zheng and Pollock, \{David D.\} and Albert, \{Victor A.\} and Shuaicheng Li and Mitsuyasu Hasebe",

year = "2017",

month = feb,

day = "6",

doi = "10.1038/s41559-016-0059",

language = "English",

volume = "1",

journal = "Nature Ecology and Evolution",

issn = "2397-334X",

publisher = "Nature Research",

number = "3",

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Fukushima, K, Fang, X, Alvarez-Ponce, D, Cai, H, Carretero-Paulet, L, Chen, C, Chang, TH, Farr, KM, Fujita, T, Hiwatashi, Y, Hoshi, Y, Imai, T, Kasahara, M, Librado, P, Mao, L, Mori, H, Nishiyama, T, Nozawa, M, Pálfalvi, G, Pollard, ST, Rozas, J, Sánchez-Gracia, A, Sankoff, D, Shibata, TF, Shigenobu, S, Sumikawa, N, Uzawa, T, Xie, M, Zheng, C, Pollock, DD, Albert, VA, Li, S & Hasebe, M 2017, 'Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory', Nature Ecology and Evolution, vol. 1, no. 3, 0059. https://doi.org/10.1038/s41559-016-0059

TY - JOUR

T1 - Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

AU - Fukushima, Kenji

AU - Fang, Xiaodong

AU - Alvarez-Ponce, David

AU - Cai, Huimin

AU - Carretero-Paulet, Lorenzo

AU - Chen, Cui

AU - Chang, Tien Hao

AU - Farr, Kimberly M.

AU - Fujita, Tomomichi

AU - Hiwatashi, Yuji

AU - Hoshi, Yoshikazu

AU - Imai, Takamasa

AU - Kasahara, Masahiro

AU - Librado, Pablo

AU - Mao, Likai

AU - Mori, Hitoshi

AU - Nishiyama, Tomoaki

AU - Nozawa, Masafumi

AU - Pálfalvi, Gergo

AU - Pollard, Stephen T.

AU - Rozas, Julio

AU - Sánchez-Gracia, Alejandro

AU - Sankoff, David

AU - Shibata, Tomoko F.

AU - Shigenobu, Shuji

AU - Sumikawa, Naomi

AU - Uzawa, Taketoshi

AU - Xie, Meiying

AU - Zheng, Chunfang

AU - Pollock, David D.

AU - Albert, Victor A.

AU - Li, Shuaicheng

AU - Hasebe, Mitsuyasu

PY - 2017/2/6

Y1 - 2017/2/6

N2 - Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.

AB - Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.

UR - https://www.scopus.com/pages/publications/85022052445

U2 - 10.1038/s41559-016-0059

DO - 10.1038/s41559-016-0059

M3 - Article

C2 - 28812732

AN - SCOPUS:85022052445

SN - 2397-334X

VL - 1

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 3

M1 - 0059

ER -

Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

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