On the hybrid origin of the C2 Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages

Delphine T. Tefarikis; Diego Morales Briones; Ya Yang; Gerald Edwards; Gudrun Kadereit

doi:10.1111/nph.18098

On the hybrid origin of the C₂ Salsola divaricata agg. (Amaranthaceae) from C₃ and C₄ parental lineages

Delphine T. Tefarikis, Diego Morales Briones, Ya Yang, Gerald Edwards, Gudrun Kadereit

Plant and Microbial Biology

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

6 Scopus citations

Abstract

C₂ photosynthesis is characterised using recapturing photorespiratory CO₂ by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C₃ and C₄ photosynthesis. C₂ can be interpreted as an evolutionary precursor of C₄ and/or as the result of hybridisation between a C₃ and C₄ lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C₂) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C₄-like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C₄-like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C₂ photosynthesis in the Salsola divaricata agg. combines traits inherited from its C₃ and C₄ parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.

Original language	English (US)
Pages (from-to)	1876-1890
Number of pages	15
Journal	New Phytologist
Volume	234
Issue number	5
DOIs	https://doi.org/10.1111/nph.18098
State	Published - Jun 2022

Bibliographical note

Funding Information:
Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9-1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of Salsola divaricata agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil González, F. Hernández, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding Information:
Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9‐1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil González, F. Hernández, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Salsola divaricata

Publisher Copyright:
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

Keywords

Amaranthaceae
C photosynthesis
CO compensation point
Salsola divaricata agg
carbon isotope values
hybridisation events
phosphoenolpyruvate carboxylase
phylogenomics

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1111/nph.18098

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@article{128de7bcd11e4342a03da660388fadea,

title = "On the hybrid origin of the C2 Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages",

abstract = "C2 photosynthesis is characterised using recapturing photorespiratory CO2 by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C3 and C4 photosynthesis. C2 can be interpreted as an evolutionary precursor of C4 and/or as the result of hybridisation between a C3 and C4 lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C2) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C4-like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C4-like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C2 photosynthesis in the Salsola divaricata agg. combines traits inherited from its C3 and C4 parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.",

keywords = "Amaranthaceae, C photosynthesis, CO compensation point, Salsola divaricata agg, carbon isotope values, hybridisation events, phosphoenolpyruvate carboxylase, phylogenomics",

author = "Tefarikis, {Delphine T.} and {Morales Briones}, Diego and Ya Yang and Gerald Edwards and Gudrun Kadereit",

note = "Funding Information: Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9-1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of Salsola divaricata agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil Gonz{\'a}lez, F. Hern{\'a}ndez, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Funding Information: Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9‐1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil Gonz{\'a}lez, F. Hern{\'a}ndez, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Salsola divaricata Publisher Copyright: {\textcopyright} 2022 The Authors. New Phytologist {\textcopyright} 2022 New Phytologist Foundation.",

year = "2022",

month = jun,

doi = "10.1111/nph.18098",

language = "English (US)",

volume = "234",

pages = "1876--1890",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "5",

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TY - JOUR

T1 - On the hybrid origin of the C2 Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages

AU - Tefarikis, Delphine T.

AU - Morales Briones, Diego

AU - Yang, Ya

AU - Edwards, Gerald

AU - Kadereit, Gudrun

N1 - Funding Information: Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9-1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of Salsola divaricata agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil González, F. Hernández, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Funding Information: Funding for this project came from the German Science Foundation (Deutsche Forschungsgemeinschaft e.V.; DFG grant no. KA1816/9‐1) and the University of Minnesota Twin Cities, St. Paul, MN, USA. We thank the collectors of seeds of agg. for their great help in starting this project, in particular R. Barone, V. Boehlke, H. Freitag, J. Gil González, F. Hernández, M. Olangua Corral, S. Scholz and E. Voznesenskaya. We are grateful to C. Wild for cultivating and maintaining the plants for this project. For conducting a part of the carbon isotope measurements, we thank M. Maus (Geology Department, University of Mainz, Germany). The Minnesota Supercomputing Institute provided access to computational resources. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Salsola divaricata Publisher Copyright: © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

PY - 2022/6

Y1 - 2022/6

N2 - C2 photosynthesis is characterised using recapturing photorespiratory CO2 by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C3 and C4 photosynthesis. C2 can be interpreted as an evolutionary precursor of C4 and/or as the result of hybridisation between a C3 and C4 lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C2) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C4-like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C4-like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C2 photosynthesis in the Salsola divaricata agg. combines traits inherited from its C3 and C4 parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.

AB - C2 photosynthesis is characterised using recapturing photorespiratory CO2 by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C3 and C4 photosynthesis. C2 can be interpreted as an evolutionary precursor of C4 and/or as the result of hybridisation between a C3 and C4 lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C2) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C4-like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C4-like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C2 photosynthesis in the Salsola divaricata agg. combines traits inherited from its C3 and C4 parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.

KW - Amaranthaceae

KW - C photosynthesis

KW - CO compensation point

KW - Salsola divaricata agg

KW - carbon isotope values

KW - hybridisation events

KW - phosphoenolpyruvate carboxylase

KW - phylogenomics

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