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

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

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Abstract

Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus 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 stomatal function are conserved in Anthoceros and upregulated 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 that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

Original language	English (US)
Pages (from-to)	259-272
Number of pages	14
Journal	Nature plants
Volume	6
Issue number	3
DOIs	https://doi.org/10.1038/s41477-020-0618-2
State	Published - Mar 1 2020

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Plant Science

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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., Blázquez, M. A., Cheng, S., Cuming, A. C., de Vries, J., de Vries, S., Delaux, P. M., Diop, I. S., Harrison, C. J., Hauser, D., Hernández-García, J., ... Szövényi, P. (2020). Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nature plants, 6(3), 259-272. https://doi.org/10.1038/s41477-020-0618-2

Li, FW, Nishiyama, T, Waller, M, Frangedakis, E, Keller, J, Li, Z, Fernandez-Pozo, N, Barker, MS, Bennett, T, Blázquez, MA, Cheng, S, Cuming, AC, de Vries, J, de Vries, S, Delaux, PM, Diop, IS, Harrison, CJ, Hauser, D, Hernández-García, J, Kirbis, A, Meeks, JC, Monte, I, Mutte, SK, Neubauer, A, Quandt, D, Robison, T, Shimamura, M, Rensing, SA, Villarreal, JC, Weijers, D, Wicke, S, Wong, GKS, Sakakibara, K & Szövényi, P 2020, 'Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts', Nature plants, vol. 6, no. 3, pp. 259-272. https://doi.org/10.1038/s41477-020-0618-2

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

abstract = "Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus 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 stomatal function are conserved in Anthoceros and upregulated 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 that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.",

author = "Li, {Fay Wei} and Tomoaki Nishiyama and Manuel Waller and Eftychios Frangedakis and Jean Keller and Zheng Li and Noe Fernandez-Pozo and Barker, {Michael S.} and Tom Bennett and Bl{\'a}zquez, {Miguel A.} and Shifeng Cheng and Cuming, {Andrew C.} and {de Vries}, Jan and {de Vries}, Sophie and Delaux, {Pierre Marc} and Diop, {Issa S.} and Harrison, {C. Jill} and Duncan Hauser and Jorge Hern{\'a}ndez-Garc{\'i}a and Alexander Kirbis and Meeks, {John C.} and Isabel Monte and Mutte, {Sumanth K.} and Anna Neubauer and Dietmar Quandt and Tanner Robison and Masaki Shimamura and Rensing, {Stefan A.} and Villarreal, {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",

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

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AU - Li, Fay Wei

AU - Nishiyama, Tomoaki

AU - Waller, Manuel

AU - Frangedakis, Eftychios

AU - Keller, Jean

AU - Li, Zheng

AU - Fernandez-Pozo, Noe

AU - Barker, Michael S.

AU - Bennett, Tom

AU - Blázquez, Miguel A.

AU - Cheng, Shifeng

AU - Cuming, Andrew C.

AU - de Vries, Jan

AU - de Vries, Sophie

AU - Delaux, Pierre Marc

AU - Diop, Issa S.

AU - Harrison, C. Jill

AU - Hauser, Duncan

AU - Hernández-García, Jorge

AU - Kirbis, Alexander

AU - Meeks, John C.

AU - Monte, Isabel

AU - Mutte, Sumanth K.

AU - Neubauer, Anna

AU - Quandt, Dietmar

AU - Robison, Tanner

AU - Shimamura, Masaki

AU - Rensing, Stefan A.

AU - Villarreal, Juan Carlos

AU - Weijers, Dolf

AU - Wicke, Susann

AU - Wong, Gane K.S.

AU - Sakakibara, Keiko

AU - Szövényi, Péter

PY - 2020/3/1

Y1 - 2020/3/1

N2 - Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus 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 stomatal function are conserved in Anthoceros and upregulated 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 that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

AB - Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus 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 stomatal function are conserved in Anthoceros and upregulated 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 that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

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VL - 6

SP - 259

EP - 272

JO - Nature plants

JF - Nature plants

IS - 3

ER -

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

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