Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

Fay-Wei Li; Tomaoki Nishiyama; Manuel Waller; Eftychios Frangedakis; Jean Keller; Zheng Li; Noe Fernandez-Pozo; Michael S Barker; Tom A Bennett; Miguel A Blazquez; Shifeng Cheng; Andrew Cuming; Jan de Vries; Sophie de Vries; Pierre-Marc Delaux; Issa S Diop; C Jill Harrison; Duncan Hauser; Jorge Hernandez-Garcia; Alexander Kirbis; John Meeks; Isabel Monte; Sumanth K Mutte; Anna Neubauer; Dietmar Quandt; Tanner Robison; Masaki Shimamura; Stefan Rensing; Juan Carlos Villareal; Dolf Weijers; Susann Wicke; Gane K-S  Wong; Keiko Sakakibara; Péter Szövényi

doi:10.1038/s41477-020-0618-2

Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

Fay-Wei Li, Tomaoki Nishiyama, Manuel Waller, Eftychios Frangedakis, Jean Keller, Zheng Li, Noe Fernandez-Pozo, Michael S Barker, Tom A Bennett, Miguel A Blazquez, Shifeng Cheng, Andrew Cuming, Jan de Vries, Sophie de Vries, Pierre-Marc Delaux, Issa S Diop, C Jill Harrison, Duncan Hauser, Jorge Hernandez-Garcia, Alexander KirbisJohn Meeks, Isabel Monte, Sumanth K Mutte, Anna Neubauer, Dietmar Quandt, Tanner Robison, Masaki Shimamura, Stefan Rensing, Juan Carlos Villareal, Dolf Weijers, Susann Wicke, Gane K-S Wong, Keiko Sakakibara, Péter Szövényi^*

^*Corresponding author for this work

School of Biological Sciences

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Abstract

Hornworts are a bryophyte lineage that diverged from other extant land plants >400 million years ago and bear unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis, and pyrenoid-based carbon-concentrating mechanism (CCM). Here we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses placed hornworts sister to liverworts+mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomata function are conserved in Anthoceros and up-regulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis, and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

Original language	English
Pages (from-to)	259–272
Journal	Nature Plants
Volume	6
DOIs	https://doi.org/10.1038/s41477-020-0618-2
Publication status	Published - 13 Mar 2020

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Li, F.-W., Nishiyama, T., Waller, M., Frangedakis, E., Keller, J., Li, Z., Fernandez-Pozo, N., Barker, M. S., Bennett, T. A., Blazquez, M. A., Cheng, S., Cuming, A., de Vries, J., de Vries, S., Delaux, P.-M., Diop, I. S., Harrison, C. J., Hauser, D., Hernandez-Garcia, J., ... Szövényi, P. (2020). Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nature Plants, 6, 259–272. https://doi.org/10.1038/s41477-020-0618-2

@article{a9ed6f37821e41bba95c2b545e48a03e,

title = "Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts",

abstract = "Hornworts are a bryophyte lineage that diverged from other extant land plants >400 million years ago and bear unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis, and pyrenoid-based carbon-concentrating mechanism (CCM). Here we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses placed hornworts sister to liverworts+mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomata function are conserved in Anthoceros and up-regulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis, and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.",

author = "Fay-Wei Li and Tomaoki Nishiyama and Manuel Waller and Eftychios Frangedakis and Jean Keller and Zheng Li and Noe Fernandez-Pozo and Barker, {Michael S} and Bennett, {Tom A} and Blazquez, {Miguel A} and Shifeng Cheng and Andrew Cuming and {de Vries}, Jan and {de Vries}, Sophie and Pierre-Marc Delaux and Diop, {Issa S} and Harrison, {C Jill} and Duncan Hauser and Jorge Hernandez-Garcia and Alexander Kirbis and John Meeks and Isabel Monte and Mutte, {Sumanth K} and Anna Neubauer and Dietmar Quandt and Tanner Robison and Masaki Shimamura and Stefan Rensing and Villareal, {Juan Carlos} and Dolf Weijers and Susann Wicke and Wong, {Gane K-S} and Keiko Sakakibara and P{\'e}ter Sz{\"o}v{\'e}nyi",

year = "2020",

month = mar,

day = "13",

doi = "10.1038/s41477-020-0618-2",

language = "English",

volume = "6",

pages = "259–272",

journal = "Nature Plants",

issn = "2055-026X",

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Li, F-W, Nishiyama, T, Waller, M, Frangedakis, E, Keller, J, Li, Z, Fernandez-Pozo, N, Barker, MS, Bennett, TA, Blazquez, MA, Cheng, S, Cuming, A, de Vries, J, de Vries, S, Delaux, P-M, Diop, IS, Harrison, CJ, Hauser, D, Hernandez-Garcia, J, Kirbis, A, Meeks, J, Monte, I, Mutte, SK, Neubauer, A, Quandt, D, Robison, T, Shimamura, M, Rensing, S, Villareal, JC, Weijers, D, Wicke, S, Wong, GK-S, Sakakibara, K & Szövényi, P 2020, 'Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts', Nature Plants, vol. 6, pp. 259–272. https://doi.org/10.1038/s41477-020-0618-2

TY - JOUR

T1 - Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

AU - Li, Fay-Wei

AU - Nishiyama, Tomaoki

AU - Waller, Manuel

AU - Frangedakis, Eftychios

AU - Keller, Jean

AU - Li, Zheng

AU - Fernandez-Pozo, Noe

AU - Barker, Michael S

AU - Bennett, Tom A

AU - Blazquez, Miguel A

AU - Cheng, Shifeng

AU - Cuming, Andrew

AU - de Vries, Jan

AU - de Vries, Sophie

AU - Delaux, Pierre-Marc

AU - Diop, Issa S

AU - Harrison, C Jill

AU - Hauser, Duncan

AU - Hernandez-Garcia, Jorge

AU - Kirbis, Alexander

AU - Meeks, John

AU - Monte, Isabel

AU - Mutte, Sumanth K

AU - Neubauer, Anna

AU - Quandt, Dietmar

AU - Robison, Tanner

AU - Shimamura, Masaki

AU - Rensing, Stefan

AU - Villareal, Juan Carlos

AU - Weijers, Dolf

AU - Wicke, Susann

AU - Wong, Gane K-S

AU - Sakakibara, Keiko

AU - Szövényi, Péter

PY - 2020/3/13

Y1 - 2020/3/13

N2 - Hornworts are a bryophyte lineage that diverged from other extant land plants >400 million years ago and bear unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis, and pyrenoid-based carbon-concentrating mechanism (CCM). Here we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses placed hornworts sister to liverworts+mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomata function are conserved in Anthoceros and up-regulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis, and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

AB - Hornworts are a bryophyte lineage that diverged from other extant land plants >400 million years ago and bear unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis, and pyrenoid-based carbon-concentrating mechanism (CCM). Here we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses placed hornworts sister to liverworts+mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomata function are conserved in Anthoceros and up-regulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis, and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

U2 - 10.1038/s41477-020-0618-2

DO - 10.1038/s41477-020-0618-2

M3 - Article (Academic Journal)

C2 - 32170292

SN - 2055-026X

VL - 6

SP - 259

EP - 272

JO - Nature Plants

JF - Nature Plants

ER -

Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

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