Abstract
C4 photosynthesis is a complex trait that evolved from its ancestral C3 photosynthesis by recruiting pre-existing genes. These co-opted genes were changed in many aspects compared to their counterparts in C3 species. Most of the evolutionary changes of the C4 shuttle enzymes are well characterized, however, evolutionary changes for the recruited metabolite transporters are less studied. Here we analyzed the evolutionary changes of the shuttle enzyme phosphoenolpyruvate (PEP) transporter (PPT) during its recruitment from C3 to C4 photosynthesis. Our analysis showed that among the two PPT paralogs PPT1 and PPT2, PPT1 was the copy recruited for C4 photosynthesis in multiple C4 lineages. During C4 evolution, PPT1 gained increased transcript abundance, shifted its expression from predominantly in root to in leaf and from bundle sheath cell to mesophyll cell, and gained more rapid and long-lasting responsiveness to light. Modifications occurred in both regulatory and coding regions in C4 PPT1 as compared to C3 PPT1, however, the PEP transporting function of PPT1 remained. We found that PPT1 of a Flaveria C4 species recruited a MEM1 B submodule in the promoter region, which might be related to the increased transcript abundance of PPT1 in C4 mesophyll cells. The case study of PPT further suggested that high transcript abundance in a proper location is of high priority for PPT to support C4 function.
Highlights
Compared to C3 photosynthesis, C4 photosynthesis has higher light, nitrogen, and water using efficiencies (Sage and Zhu, 2011)
Comparisons of genes involved in C4 photosynthesis in C4 species and their counterparts in C3 species showed that these genes were modified in different aspects (Gowik and Westhoff, 2011), e.g., increasing transcript abundance [see review in (Hibberd and Covshoff, 2010)]; acquiring cell specific expression (Hatch and Osmond, 1976; Aubry et al, 2014); gaining modifications in protein coding regions resulting in suitability for C4 photosynthesis (Blasing et al, 2000; Paulus et al, 2013); obtaining new cis-elements (Gowik et al, 2004; Williams et al, 2016; Gupta et al, 2020); and having more copies (Bianconi et al, 2018)
In an example study in Flaveria, we found that PPT1 from a C4 species gained a MEM1 B submodule, which might contribute to the changes in transcriptional properties of PPT1 in C4 species
Summary
Compared to C3 photosynthesis, C4 photosynthesis has higher light, nitrogen, and water using efficiencies (Sage and Zhu, 2011). It achieves these superior properties through a CO2 concentrating mechanism operating in a specialized leaf anatomical feature termed “Kranz anatomy” (Hatch, 1987). Comparisons of genes involved in C4 photosynthesis in C4 species and their counterparts in C3 species showed that these genes were modified in different aspects (Gowik and Westhoff, 2011), e.g., increasing transcript abundance [see review in (Hibberd and Covshoff, 2010)]; acquiring cell specific expression (Hatch and Osmond, 1976; Aubry et al, 2014); gaining modifications in protein coding regions resulting in suitability for C4 photosynthesis (Blasing et al, 2000; Paulus et al, 2013); obtaining new cis-elements (Gowik et al, 2004; Williams et al, 2016; Gupta et al, 2020); and having more copies (Bianconi et al, 2018)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
