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 Sanz; Likai Mao; Hitoshi Mori; Tomoaki Nishiyama; Masafumi Nozawa; Gergő 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 Sanz, Likai Mao, Hitoshi Mori, Tomoaki Nishiyama, Masafumi Nozawa, Gergő Pálfalvi, Stephen T. PollardJulio 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

^*Corresponding author for this work

51 Citations (Scopus)

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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
Number of pages	9
ISSN	2397-334X
DOIs	https://doi.org/10.1038/s41559-016-0059
Publication status	Published - 6 Feb 2017

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Fukushima_2017_Genome_of_the_pitcherFinal published version, 1.54 MBLicence: CC BY

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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., Sanz, P. L., 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), [0059]. https://doi.org/10.1038/s41559-016-0059

Fukushima, K, Fang, X, Alvarez-Ponce, D, Cai, H, Carretero-Paulet, L, Chen, C, Chang, T-H, Farr, KM, Fujita, T, Hiwatashi, Y, Hoshi, Y, Imai, T, Kasahara, M, Sanz, PL, 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

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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.",

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AU - Hoshi, Yoshikazu

AU - Imai, Takamasa

AU - Kasahara, Masahiro

AU - Sanz, Pablo Librado

AU - Mao, Likai

AU - Mori, Hitoshi

AU - Nishiyama, Tomoaki

AU - Nozawa, Masafumi

AU - Pálfalvi, Gergő

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

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

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