Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

John L. Bowman; Takayuki Kohchi; Katsuyuki T. Yamato; Jerry Jenkins; Shengqiang Shu; Kimitsune Ishizaki; Shohei Yamaoka; Ryuichi Nishihama; Yasukazu Nakamura; Frédéric Berger; Catherine Adam; Shiori Sugamata Aki; Felix Althoff; Takashi Araki; Mario A. Arteaga-Vazquez; Sureshkumar Balasubrmanian; Kerrie Barry; Diane Bauer; Christian R. Boehm; Liam Briginshaw; Juan Caballero-Perez; Bruno Catarino; Feng Chen; Shota Chiyoda; Mansi Chovatia; Kevin M. Davies; Mihails Delmans; Taku Demura; Tom Dierschke; Liam Dolan; Ana E. Dorantes-Acosta; D. Magnus Eklund; Stevie N. Florent; Eduardo Flores-Sandoval; Asao Fujiyama; Hideya Fukuzawa; Bence Galik; Daniel Grimanelli; Jane Grimwood; Ueli Grossniklaus; Takahiro Hamada; Jim Haseloff; Alexander J. Hetherington; Asuka Higo; Yuki Hirakawa; Hope N. Hundley; Yoko Ikeda; Keisuke Inoue; Shin ichiro Inoue; Sakiko Ishida; Qidong Jia; Mitsuru Kakita; Takehiko Kanazawa; Yosuke Kawai; Tomokazu Kawashima; Megan Kennedy; Keita Kinose; Toshinori Kinoshita; Yuji Kohara; Eri Koide; Kenji Komatsu; Sarah Kopischke; Minoru Kubo; Junko Kyozuka; Ulf Lagercrantz; Shih Shun Lin; Erika Lindquist; Anna M. Lipzen; Chia Wei Lu; Efraín De Luna; Robert A. Martienssen; Naoki Minamino; Masaharu Mizutani; Miya Mizutani; Nobuyoshi Mochizuki; Isabel Monte; Rebecca Mosher; Hideki Nagasaki; Hirofumi Nakagami; Satoshi Naramoto; Kazuhiko Nishitani; Misato Ohtani; Takashi Okamoto; Masaki Okumura; Jeremy Phillips; Bernardo Pollak; Anke Reinders; Moritz Rövekamp; Ryosuke Sano; Shinichiro Sawa; Marc W. Schmid; Makoto Shirakawa; Roberto Solano; Alexander Spunde; Noriyuki Suetsugu; Sumio Sugano; Akifumi Sugiyama; Rui Sun; Yutaka Suzuki; Mizuki Takenaka; Daisuke Takezawa; Hirokazu Tomogane; Masayuki Tsuzuki; Takashi Ueda; Masaaki Umeda; John M. Ward; Yuichiro Watanabe; Kazufumi Yazaki; Ryusuke Yokoyama; Yoshihiro Yoshitake; Izumi Yotsui; Sabine Zachgo; Jeremy Schmutz

doi:10.1016/j.cell.2017.09.030

Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

John L. Bowman, Takayuki Kohchi, Katsuyuki T. Yamato, Jerry Jenkins, Shengqiang Shu, Kimitsune Ishizaki, Shohei Yamaoka, Ryuichi Nishihama, Yasukazu Nakamura, Frédéric Berger, Catherine Adam, Shiori Sugamata Aki, Felix Althoff, Takashi Araki, Mario A. Arteaga-Vazquez, Sureshkumar Balasubrmanian, Kerrie Barry, Diane Bauer, Christian R. Boehm, Liam BriginshawJuan Caballero-Perez, Bruno Catarino, Feng Chen, Shota Chiyoda, Mansi Chovatia, Kevin M. Davies, Mihails Delmans, Taku Demura, Tom Dierschke, Liam Dolan, Ana E. Dorantes-Acosta, D. Magnus Eklund, Stevie N. Florent, Eduardo Flores-Sandoval, Asao Fujiyama, Hideya Fukuzawa, Bence Galik, Daniel Grimanelli, Jane Grimwood, Ueli Grossniklaus, Takahiro Hamada, Jim Haseloff, Alexander J. Hetherington, Asuka Higo, Yuki Hirakawa, Hope N. Hundley, Yoko Ikeda, Keisuke Inoue, Shin ichiro Inoue, Sakiko Ishida, Qidong Jia, Mitsuru Kakita, Takehiko Kanazawa, Yosuke Kawai, Tomokazu Kawashima, Megan Kennedy, Keita Kinose, Toshinori Kinoshita, Yuji Kohara, Eri Koide, Kenji Komatsu, Sarah Kopischke, Minoru Kubo, Junko Kyozuka, Ulf Lagercrantz, Shih Shun Lin, Erika Lindquist, Anna M. Lipzen, Chia Wei Lu, Efraín De Luna, Robert A. Martienssen, Naoki Minamino, Masaharu Mizutani, Miya Mizutani, Nobuyoshi Mochizuki, Isabel Monte, Rebecca Mosher, Hideki Nagasaki, Hirofumi Nakagami, Satoshi Naramoto, Kazuhiko Nishitani, Misato Ohtani, Takashi Okamoto, Masaki Okumura, Jeremy Phillips, Bernardo Pollak, Anke Reinders, Moritz Rövekamp, Ryosuke Sano, Shinichiro Sawa, Marc W. Schmid, Makoto Shirakawa, Roberto Solano, Alexander Spunde, Noriyuki Suetsugu, Sumio Sugano, Akifumi Sugiyama, Rui Sun, Yutaka Suzuki, Mizuki Takenaka, Daisuke Takezawa, Hirokazu Tomogane, Masayuki Tsuzuki, Takashi Ueda, Masaaki Umeda, John M. Ward, Yuichiro Watanabe, Kazufumi Yazaki, Ryusuke Yokoyama, Yoshihiro Yoshitake, Izumi Yotsui, Sabine Zachgo, Jeremy Schmutz

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

941 Scopus citations

Abstract

The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PaperClip [Formula presentes] The genome of the liverwort Marchantia polymorpha sheds light on the evolution of land plants.

Original language	English
Pages (from-to)	287-304.e15
Journal	Cell
Volume	171
Issue number	2
DOIs	https://doi.org/10.1016/j.cell.2017.09.030
State	Published - Oct 5 2017

Bibliographical note

Publisher Copyright:
© 2017 The Author(s)

Funding

The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. Funding from ARC FF0561326 , DP130100177 , DP160100892 (J.L.B), MEXT KAKENHI Grant Numbers ( 15K21758 , 16H06279 , 25113001 , 25113009 [T. Kohchi], 22112514 , 24112715 , 24510272 [K.T.Y.], 15H04391 , 15H01233 , 17H06472 [K. Ishizaki], FWF grant P28320-B21 (F.B.), SNF grant 310030B_160336 (U.G.), Gates Cambridge Trust (C.R.B.), Program to Disseminate Tenure Tracking System , MEXT, Japan (Y.I.), the Marsden Fund of New Zealand grant PAF1302 (K.D.), UC MEXUS Collaborative program grant 2011-UCMEXUS-19941-44-OAC7 (M.A.A.-V, X.C., and E.D.L.), Consejo Nacional de Ciencia y Tecnología (CONACYT) grant CB-158550 (M.A.A.-V.), COSEAMX1 JEAI EPIMAIZE , Universidad Veracruzana (M.A.A.-V. and D.G.), CONACYT grant CB-158561 (A.E.D.A.), Newton Fund grant RG79985 (M.A.A.-V. and J.H.), and Universidad Veracruzana - Cuerpo Académico CA-UVER-234 , Marie Sklodowska-Curie action ( #658900 ) (D.G.) is acknowledged. We thank Sandra K. Floyd for DNA and RNA isolation; David Powell, Kathryn Hodgins, and Xuemei Chen for bioinformatics assistance; and Kanako Takeda, Manami Miyazaki, Takumi Kondoh, Yuiri Sowa, Yuma Hibi, Ryo Hirai, Motoyoshi Nakamura, Jun Inoue, Tatsuya Hasegawa, Mihoko Kobayashi, Kyoko Miyashita, and Taisuke Togawa for isolation of X-linked markers. We apologize to those researchers whose works we consulted but were unable to cite due to lack of space.

Funders	Funder number
Gates Cambridge Trust
Office of Science Programs
Japan Society for the Promotion of Science	17H03691, 17H07333, 16K07389, 16K07398, 16K13087, 25221103, 15H04628, 16H06279, 17K19412, 15KK0254, 15H04386, 15H04382, 16J04519, 15K07104, 17K19374, 16K14742, 17H03967, 17K17595, 15H04391
University of California Institute for Mexico and the United States	2011-UCMEXUS-19941-44-OAC7
Marsden Fund of New Zealand	PAF1302
U.S. Department of Energy EPSCoR	DE-AC02-05CH11231
Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica	CB-158550, CB-158561
Australian Research Council	DP160100892, FF0561326, DP130100177
Newton Fund	RG79985
Austrian Science Fund/FWF	P 28320, P28320-B21
Biotechnology and Biological Sciences Research Council	BB/L014130/1, BB/M018768/1
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	160336, 310030B_160336
Ministry of Education, Culture, Sports, Science and Technology	15H01233, 24510272, 15K21758, 25113009, 25113001, 17H06472, 24112715, 22112514
Horizon 2020 Framework Programme	658900

Keywords

Marchantia polymorpha
auxin
charophycean algae
land plant evolution
sex chromosome

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

Access to Document

10.1016/j.cell.2017.09.030

Cite this

Bowman, J. L., Kohchi, T., Yamato, K. T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., Adam, C., Aki, S. S., Althoff, F., Araki, T., Arteaga-Vazquez, M. A., Balasubrmanian, S., Barry, K., Bauer, D., Boehm, C. R., ... Schmutz, J. (2017). Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. Cell, 171(2), 287-304.e15. https://doi.org/10.1016/j.cell.2017.09.030

@article{8dc774a87f444d78a1c176f184674450,

title = "Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome",

abstract = "The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PaperClip [Formula presentes] The genome of the liverwort Marchantia polymorpha sheds light on the evolution of land plants.",

keywords = "Marchantia polymorpha, auxin, charophycean algae, land plant evolution, sex chromosome",

author = "Bowman, \{John L.\} and Takayuki Kohchi and Yamato, \{Katsuyuki T.\} and Jerry Jenkins and Shengqiang Shu and Kimitsune Ishizaki and Shohei Yamaoka and Ryuichi Nishihama and Yasukazu Nakamura and Fr{\'e}d{\'e}ric Berger and Catherine Adam and Aki, \{Shiori Sugamata\} and Felix Althoff and Takashi Araki and Arteaga-Vazquez, \{Mario A.\} and Sureshkumar Balasubrmanian and Kerrie Barry and Diane Bauer and Boehm, \{Christian R.\} and Liam Briginshaw and Juan Caballero-Perez and Bruno Catarino and Feng Chen and Shota Chiyoda and Mansi Chovatia and Davies, \{Kevin M.\} and Mihails Delmans and Taku Demura and Tom Dierschke and Liam Dolan and Dorantes-Acosta, \{Ana E.\} and Eklund, \{D. Magnus\} and Florent, \{Stevie N.\} and Eduardo Flores-Sandoval and Asao Fujiyama and Hideya Fukuzawa and Bence Galik and Daniel Grimanelli and Jane Grimwood and Ueli Grossniklaus and Takahiro Hamada and Jim Haseloff and Hetherington, \{Alexander J.\} and Asuka Higo and Yuki Hirakawa and Hundley, \{Hope N.\} and Yoko Ikeda and Keisuke Inoue and Inoue, \{Shin ichiro\} and Sakiko Ishida and Qidong Jia and Mitsuru Kakita and Takehiko Kanazawa and Yosuke Kawai and Tomokazu Kawashima and Megan Kennedy and Keita Kinose and Toshinori Kinoshita and Yuji Kohara and Eri Koide and Kenji Komatsu and Sarah Kopischke and Minoru Kubo and Junko Kyozuka and Ulf Lagercrantz and Lin, \{Shih Shun\} and Erika Lindquist and Lipzen, \{Anna M.\} and Lu, \{Chia Wei\} and \{De Luna\}, Efra{\'i}n and Martienssen, \{Robert A.\} and Naoki Minamino and Masaharu Mizutani and Miya Mizutani and Nobuyoshi Mochizuki and Isabel Monte and Rebecca Mosher and Hideki Nagasaki and Hirofumi Nakagami and Satoshi Naramoto and Kazuhiko Nishitani and Misato Ohtani and Takashi Okamoto and Masaki Okumura and Jeremy Phillips and Bernardo Pollak and Anke Reinders and Moritz R{\"o}vekamp and Ryosuke Sano and Shinichiro Sawa and Schmid, \{Marc W.\} and Makoto Shirakawa and Roberto Solano and Alexander Spunde and Noriyuki Suetsugu and Sumio Sugano and Akifumi Sugiyama and Rui Sun and Yutaka Suzuki and Mizuki Takenaka and Daisuke Takezawa and Hirokazu Tomogane and Masayuki Tsuzuki and Takashi Ueda and Masaaki Umeda and Ward, \{John M.\} and Yuichiro Watanabe and Kazufumi Yazaki and Ryusuke Yokoyama and Yoshihiro Yoshitake and Izumi Yotsui and Sabine Zachgo and Jeremy Schmutz",

note = "Publisher Copyright: {\textcopyright} 2017 The Author(s)",

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doi = "10.1016/j.cell.2017.09.030",

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Bowman, JL, Kohchi, T, Yamato, KT, Jenkins, J, Shu, S, Ishizaki, K, Yamaoka, S, Nishihama, R, Nakamura, Y, Berger, F, Adam, C, Aki, SS, Althoff, F, Araki, T, Arteaga-Vazquez, MA, Balasubrmanian, S, Barry, K, Bauer, D, Boehm, CR, Briginshaw, L, Caballero-Perez, J, Catarino, B, Chen, F, Chiyoda, S, Chovatia, M, Davies, KM, Delmans, M, Demura, T, Dierschke, T, Dolan, L, Dorantes-Acosta, AE, Eklund, DM, Florent, SN, Flores-Sandoval, E, Fujiyama, A, Fukuzawa, H, Galik, B, Grimanelli, D, Grimwood, J, Grossniklaus, U, Hamada, T, Haseloff, J, Hetherington, AJ, Higo, A, Hirakawa, Y, Hundley, HN, Ikeda, Y, Inoue, K, Inoue, SI, Ishida, S, Jia, Q, Kakita, M, Kanazawa, T, Kawai, Y, Kawashima, T, Kennedy, M, Kinose, K, Kinoshita, T, Kohara, Y, Koide, E, Komatsu, K, Kopischke, S, Kubo, M, Kyozuka, J, Lagercrantz, U, Lin, SS, Lindquist, E, Lipzen, AM, Lu, CW, De Luna, E, Martienssen, RA, Minamino, N, Mizutani, M, Mizutani, M, Mochizuki, N, Monte, I, Mosher, R, Nagasaki, H, Nakagami, H, Naramoto, S, Nishitani, K, Ohtani, M, Okamoto, T, Okumura, M, Phillips, J, Pollak, B, Reinders, A, Rövekamp, M, Sano, R, Sawa, S, Schmid, MW, Shirakawa, M, Solano, R, Spunde, A, Suetsugu, N, Sugano, S, Sugiyama, A, Sun, R, Suzuki, Y, Takenaka, M, Takezawa, D, Tomogane, H, Tsuzuki, M, Ueda, T, Umeda, M, Ward, JM, Watanabe, Y, Yazaki, K, Yokoyama, R, Yoshitake, Y, Yotsui, I, Zachgo, S & Schmutz, J 2017, 'Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome', Cell, vol. 171, no. 2, pp. 287-304.e15. https://doi.org/10.1016/j.cell.2017.09.030

TY - JOUR

T1 - Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

AU - Bowman, John L.

AU - Kohchi, Takayuki

AU - Yamato, Katsuyuki T.

AU - Jenkins, Jerry

AU - Shu, Shengqiang

AU - Ishizaki, Kimitsune

AU - Yamaoka, Shohei

AU - Nishihama, Ryuichi

AU - Nakamura, Yasukazu

AU - Berger, Frédéric

AU - Adam, Catherine

AU - Aki, Shiori Sugamata

AU - Althoff, Felix

AU - Araki, Takashi

AU - Arteaga-Vazquez, Mario A.

AU - Balasubrmanian, Sureshkumar

AU - Barry, Kerrie

AU - Bauer, Diane

AU - Boehm, Christian R.

AU - Briginshaw, Liam

AU - Caballero-Perez, Juan

AU - Catarino, Bruno

AU - Chen, Feng

AU - Chiyoda, Shota

AU - Chovatia, Mansi

AU - Davies, Kevin M.

AU - Delmans, Mihails

AU - Demura, Taku

AU - Dierschke, Tom

AU - Dolan, Liam

AU - Dorantes-Acosta, Ana E.

AU - Eklund, D. Magnus

AU - Florent, Stevie N.

AU - Flores-Sandoval, Eduardo

AU - Fujiyama, Asao

AU - Fukuzawa, Hideya

AU - Galik, Bence

AU - Grimanelli, Daniel

AU - Grimwood, Jane

AU - Grossniklaus, Ueli

AU - Hamada, Takahiro

AU - Haseloff, Jim

AU - Hetherington, Alexander J.

AU - Higo, Asuka

AU - Hirakawa, Yuki

AU - Hundley, Hope N.

AU - Ikeda, Yoko

AU - Inoue, Keisuke

AU - Inoue, Shin ichiro

AU - Ishida, Sakiko

AU - Jia, Qidong

AU - Kakita, Mitsuru

AU - Kanazawa, Takehiko

AU - Kawai, Yosuke

AU - Kawashima, Tomokazu

AU - Kennedy, Megan

AU - Kinose, Keita

AU - Kinoshita, Toshinori

AU - Kohara, Yuji

AU - Koide, Eri

AU - Komatsu, Kenji

AU - Kopischke, Sarah

AU - Kubo, Minoru

AU - Kyozuka, Junko

AU - Lagercrantz, Ulf

AU - Lin, Shih Shun

AU - Lindquist, Erika

AU - Lipzen, Anna M.

AU - Lu, Chia Wei

AU - De Luna, Efraín

AU - Martienssen, Robert A.

AU - Minamino, Naoki

AU - Mizutani, Masaharu

AU - Mizutani, Miya

AU - Mochizuki, Nobuyoshi

AU - Monte, Isabel

AU - Mosher, Rebecca

AU - Nagasaki, Hideki

AU - Nakagami, Hirofumi

AU - Naramoto, Satoshi

AU - Nishitani, Kazuhiko

AU - Ohtani, Misato

AU - Okamoto, Takashi

AU - Okumura, Masaki

AU - Phillips, Jeremy

AU - Pollak, Bernardo

AU - Reinders, Anke

AU - Rövekamp, Moritz

AU - Sano, Ryosuke

AU - Sawa, Shinichiro

AU - Schmid, Marc W.

AU - Shirakawa, Makoto

AU - Solano, Roberto

AU - Spunde, Alexander

AU - Suetsugu, Noriyuki

AU - Sugano, Sumio

AU - Sugiyama, Akifumi

AU - Sun, Rui

AU - Suzuki, Yutaka

AU - Takenaka, Mizuki

AU - Takezawa, Daisuke

AU - Tomogane, Hirokazu

AU - Tsuzuki, Masayuki

AU - Ueda, Takashi

AU - Umeda, Masaaki

AU - Ward, John M.

AU - Watanabe, Yuichiro

AU - Yazaki, Kazufumi

AU - Yokoyama, Ryusuke

AU - Yoshitake, Yoshihiro

AU - Yotsui, Izumi

AU - Zachgo, Sabine

AU - Schmutz, Jeremy

PY - 2017/10/5

Y1 - 2017/10/5

N2 - The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PaperClip [Formula presentes] The genome of the liverwort Marchantia polymorpha sheds light on the evolution of land plants.

AB - The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PaperClip [Formula presentes] The genome of the liverwort Marchantia polymorpha sheds light on the evolution of land plants.

KW - Marchantia polymorpha

KW - auxin

KW - charophycean algae

KW - land plant evolution

KW - sex chromosome

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JO - Cell

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Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

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