Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics

Adam L. Healey; Bryan Piatkowski; John T. Lovell; Avinash Sreedasyam; Sarah B. Carey; Sujan Mamidi; Shengqiang Shu; Chris Plott; Jerry Jenkins; Travis Lawrence; Blanka Aguero; Alyssa A. Carrell; Marta Nieto-Lugilde; Jayson Talag; Aaron Duffy; Sara Jawdy; Kelsey R. Carter; Lori Beth Boston; Teresa Jones; Juan Jaramillo-Chico; Alex Harkess; Kerrie Barry; Keykhosrow Keymanesh; Diane Bauer; Jane Grimwood; Lee Gunter; Jeremy Schmutz; David J. Weston; A. Jonathan Shaw

doi:10.1038/s41477-022-01333-5

Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics

Adam L. Healey, Bryan Piatkowski, John T. Lovell, Avinash Sreedasyam, Sarah B. Carey, Sujan Mamidi, Shengqiang Shu, Chris Plott, Jerry Jenkins, Travis Lawrence, Blanka Aguero, Alyssa A. Carrell, Marta Nieto-Lugilde, Jayson Talag, Aaron Duffy, Sara Jawdy, Kelsey R. Carter, Lori Beth Boston, Teresa Jones, Juan Jaramillo-ChicoAlex Harkess, Kerrie Barry, Keykhosrow Keymanesh, Diane Bauer, Jane Grimwood, Lee Gunter, Jeremy Schmutz, David J. Weston, A. Jonathan Shaw

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

27 Scopus citations

Abstract

Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates. Sphagnum (peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of two Sphagnum species: S. divinum and S. angustifolium. Sphagnum genomes show no gene colinearity with any other reference genome to date, demonstrating that Sphagnum represents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability of Sphagnum to sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.

Original language	English
Pages (from-to)	238-254
Number of pages	17
Journal	Nature Plants
Volume	9
Issue number	2
DOIs	https://doi.org/10.1038/s41477-022-01333-5
State	Published - Feb 2023

Funding

The work (proposal no. 10.46936/10.25585/60001030) (A.J.S.) conducted by the US Department of Energy (DOE) Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported under contract no. DE-AC02-05CH11231. Collection of starting Sphagnum was made possible through the SPRUCE project, which is supported by the DOE Office of Science; Biological and Environmental Research (BER); US DOE grant no. DE-AC05–00OR22725 (D.W.). Experimental work and analyses were supported by the DOE BER Early Career Research Program. Oak Ridge National Laboratory is managed by UT-Battelle LLC, for the US DOE under contract no. DE-AC05–00OR22725 (D.W.). Additional support for diversity collections and analysis by the National Science Foundation DEB-1737899 (A.J.S.), 1928514 (A.J.S.). This research used resources of the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory, which is supported by the DOE Office of Science under contract no. DE-AC05-00OR22725 (D.W.). We thank J. Carlson for submitting the genomes to the National Center for Biotechnology Information, M. Tsai for depositing data in the Sequence Read Archive (SRA), M. Kim for chloroplast contig construction and J. Sztepanacz for her assistance with regression modelling. We also thank D. Kudrna of the Arizona Genomics Institute for coordinating DNA extractions for samples. The work (proposal no. 10.46936/10.25585/60001030) (A.J.S.) conducted by the US Department of Energy (DOE) Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported under contract no. DE-AC02-05CH11231. Collection of starting Sphagnum was made possible through the SPRUCE project, which is supported by the DOE Office of Science; Biological and Environmental Research (BER); US DOE grant no. DE-AC05–00OR22725 (D.W.). Experimental work and analyses were supported by the DOE BER Early Career Research Program. Oak Ridge National Laboratory is managed by UT-Battelle LLC, for the US DOE under contract no. DE-AC05–00OR22725 (D.W.). Additional support for diversity collections and analysis by the National Science Foundation DEB-1737899 (A.J.S.), 1928514 (A.J.S.). This research used resources of the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory, which is supported by the DOE Office of Science under contract no. DE-AC05-00OR22725 (D.W.). We thank J. Carlson for submitting the genomes to the National Center for Biotechnology Information, M. Tsai for depositing data in the Sequence Read Archive (SRA), M. Kim for chloroplast contig construction and J. Sztepanacz for her assistance with regression modelling. We also thank D. Kudrna of the Arizona Genomics Institute for coordinating DNA extractions for samples.

Funders	Funder number
CADES	DE-AC05-00OR22725
DOE BER
Data Environment for Science
National Science Foundation	1928514, DEB-1737899
U.S. Department of Energy
Office of Science	DE-AC02-05CH11231
Biological and Environmental Research	DE-AC05–00OR22725
Oak Ridge National Laboratory
Joint Genome Institute
UT-Battelle

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Healey, A. L., Piatkowski, B., Lovell, J. T., Sreedasyam, A., Carey, S. B., Mamidi, S., Shu, S., Plott, C., Jenkins, J., Lawrence, T., Aguero, B., Carrell, A. A., Nieto-Lugilde, M., Talag, J., Duffy, A., Jawdy, S., Carter, K. R., Boston, L. B., Jones, T., ... Shaw, A. J. (2023). Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics. Nature Plants, 9(2), 238-254. https://doi.org/10.1038/s41477-022-01333-5

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title = "Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics",

abstract = "Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates. Sphagnum (peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of two Sphagnum species: S. divinum and S. angustifolium. Sphagnum genomes show no gene colinearity with any other reference genome to date, demonstrating that Sphagnum represents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability of Sphagnum to sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.",

author = "Healey, {Adam L.} and Bryan Piatkowski and Lovell, {John T.} and Avinash Sreedasyam and Carey, {Sarah B.} and Sujan Mamidi and Shengqiang Shu and Chris Plott and Jerry Jenkins and Travis Lawrence and Blanka Aguero and Carrell, {Alyssa A.} and Marta Nieto-Lugilde and Jayson Talag and Aaron Duffy and Sara Jawdy and Carter, {Kelsey R.} and Boston, {Lori Beth} and Teresa Jones and Juan Jaramillo-Chico and Alex Harkess and Kerrie Barry and Keykhosrow Keymanesh and Diane Bauer and Jane Grimwood and Lee Gunter and Jeremy Schmutz and Weston, {David J.} and Shaw, {A. Jonathan}",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = feb,

doi = "10.1038/s41477-022-01333-5",

language = "English",

volume = "9",

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Healey, AL, Piatkowski, B, Lovell, JT, Sreedasyam, A, Carey, SB, Mamidi, S, Shu, S, Plott, C, Jenkins, J, Lawrence, T, Aguero, B, Carrell, AA, Nieto-Lugilde, M, Talag, J, Duffy, A, Jawdy, S , Carter, KR, Boston, LB, Jones, T, Jaramillo-Chico, J, Harkess, A, Barry, K, Keymanesh, K, Bauer, D, Grimwood, J, Gunter, L, Schmutz, J, Weston, DJ & Shaw, AJ 2023, 'Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics', Nature Plants, vol. 9, no. 2, pp. 238-254. https://doi.org/10.1038/s41477-022-01333-5

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T1 - Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics

AU - Healey, Adam L.

AU - Piatkowski, Bryan

AU - Lovell, John T.

AU - Sreedasyam, Avinash

AU - Carey, Sarah B.

AU - Mamidi, Sujan

AU - Shu, Shengqiang

AU - Plott, Chris

AU - Jenkins, Jerry

AU - Lawrence, Travis

AU - Aguero, Blanka

AU - Carrell, Alyssa A.

AU - Nieto-Lugilde, Marta

AU - Talag, Jayson

AU - Duffy, Aaron

AU - Jawdy, Sara

AU - Carter, Kelsey R.

AU - Boston, Lori Beth

AU - Jones, Teresa

AU - Jaramillo-Chico, Juan

AU - Harkess, Alex

AU - Barry, Kerrie

AU - Keymanesh, Keykhosrow

AU - Bauer, Diane

AU - Grimwood, Jane

AU - Gunter, Lee

AU - Schmutz, Jeremy

AU - Weston, David J.

AU - Shaw, A. Jonathan

PY - 2023/2

Y1 - 2023/2

N2 - Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates. Sphagnum (peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of two Sphagnum species: S. divinum and S. angustifolium. Sphagnum genomes show no gene colinearity with any other reference genome to date, demonstrating that Sphagnum represents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability of Sphagnum to sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.

AB - Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates. Sphagnum (peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of two Sphagnum species: S. divinum and S. angustifolium. Sphagnum genomes show no gene colinearity with any other reference genome to date, demonstrating that Sphagnum represents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability of Sphagnum to sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.

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C2 - 36747050

AN - SCOPUS:85147492162

SN - 2055-0278

VL - 9

SP - 238

EP - 254

JO - Nature Plants

JF - Nature Plants

IS - 2

ER -

Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics

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