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A role for neutral variation in the evolution of C4 photosynthesis

Shanta Karki, HsiangChun Lin, Florence R Danila, Basel Abu-Jamous, Rita Giuliani, David M Emms, Robert A Coe, Sarah Covshoff, Helen Woodfield, Efren Bagunu, Vivek Thakur, Samart Wanchana, Inez Slamet-Loedin, Asaph B. Cousins, Julian M Hibberd, View ORCID ProfileSteven Kelly, W Paul Quick
doi: https://doi.org/10.1101/2020.05.19.104299
Shanta Karki
1, Los Baños, Philippines
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HsiangChun Lin
1, Los Baños, Philippines
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Florence R Danila
1, Los Baños, Philippines
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Basel Abu-Jamous
2Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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Rita Giuliani
3School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA
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David M Emms
2Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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Robert A Coe
1, Los Baños, Philippines
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Sarah Covshoff
4Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, United Kingdom
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Helen Woodfield
4Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, United Kingdom
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Efren Bagunu
1, Los Baños, Philippines
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Vivek Thakur
5SBDM Unit, 300 Building, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad-502324, India
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Samart Wanchana
1, Los Baños, Philippines
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Inez Slamet-Loedin
1, Los Baños, Philippines
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Asaph B. Cousins
3School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA
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Julian M Hibberd
4Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, United Kingdom
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  • For correspondence: jmh65@cam.ac.uk steven.kelly@plants.ox.ac.uk w.p.quick@irri.org
Steven Kelly
2Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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  • ORCID record for Steven Kelly
  • For correspondence: jmh65@cam.ac.uk steven.kelly@plants.ox.ac.uk w.p.quick@irri.org
W Paul Quick
1, Los Baños, Philippines
5SBDM Unit, 300 Building, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad-502324, India
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  • For correspondence: jmh65@cam.ac.uk steven.kelly@plants.ox.ac.uk w.p.quick@irri.org
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Abstract

Convergent trait evolution is a recurrent phenomenon in all domains of the tree of life. While some convergent traits are caused by simple sequence changes, many are associated with extensive changes to the sequence and regulation of large cohorts of genes. It is unknown how organisms traverse this expansive genotype space to assemble such complex convergent phenotypes. C4 photosynthesis is a paradigm of large-scale phenotypic convergence. Conceptual and mathematical models propose that C4 photosynthesis evolved from ancestral C3 photosynthesis through sequential adaptive changes. These adaptive changes could have been rapidly assembled if modifications to the activity and abundance of enzymes of the C4 cycle was neutral in C3 plants. This neutrality would enable populations of C3 plants to maintain genotypes with expression levels of C4 enzymes analogous to those in C4 species and thus enable rapid assembly of a functional C4 cycle from naturally occurring genotypes given shared environmental selection. Here we show that there is substantial natural variation in expression of genes encoding C4 cycle enzymes between natural accessions of the C3 plant Arabidopsis thaliana. We further show through targeted transgenic experiments in the C3 crop Oryza sativa, that high expression of the majority of C4 cycle enzymes in rice is neutral with respect to growth, development, biomass and photosynthesis. Thus, substantial variation in the abundance and activity of C4 cycle enzymes is permissible within the limits of operation of C3 photosynthesis and the emergence of component parts of this complex convergent trait can be facilitated by neutral variation.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted May 20, 2020.
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A role for neutral variation in the evolution of C4 photosynthesis
Shanta Karki, HsiangChun Lin, Florence R Danila, Basel Abu-Jamous, Rita Giuliani, David M Emms, Robert A Coe, Sarah Covshoff, Helen Woodfield, Efren Bagunu, Vivek Thakur, Samart Wanchana, Inez Slamet-Loedin, Asaph B. Cousins, Julian M Hibberd, Steven Kelly, W Paul Quick
bioRxiv 2020.05.19.104299; doi: https://doi.org/10.1101/2020.05.19.104299
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A role for neutral variation in the evolution of C4 photosynthesis
Shanta Karki, HsiangChun Lin, Florence R Danila, Basel Abu-Jamous, Rita Giuliani, David M Emms, Robert A Coe, Sarah Covshoff, Helen Woodfield, Efren Bagunu, Vivek Thakur, Samart Wanchana, Inez Slamet-Loedin, Asaph B. Cousins, Julian M Hibberd, Steven Kelly, W Paul Quick
bioRxiv 2020.05.19.104299; doi: https://doi.org/10.1101/2020.05.19.104299

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