AUTHOR=Khoshravesh Roxana , Stata Matt , Adachi Shunsuke , Sage Tammy L. , Sage Rowan F. 

TITLE=Evolutionary Convergence of C4 Photosynthesis: A Case Study in the Nyctaginaceae

JOURNAL=Frontiers in Plant Science

VOLUME=11

YEAR=2020

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2020.578739

DOI=10.3389/fpls.2020.578739

ISSN=1664-462X

ABSTRACT=<p>C<sub>4</sub> photosynthesis evolved over 65 times, with around 24 origins in the eudicot order Caryophyllales. In the Caryophyllales family Nyctaginaceae, the C<sub>4</sub> pathway is known in three genera of the tribe Nyctagineae: <italic>Allionia</italic>, <italic>Okenia</italic> and <italic>Boerhavia.</italic> Phylogenetically, <italic>Allionia</italic> and <italic>Boerhavia/Okenia</italic> are separated by three genera whose photosynthetic pathway is uncertain. To clarify the distribution of photosynthetic pathways in the Nyctaginaceae, we surveyed carbon isotope ratios of 159 species of the Nyctaginaceae, along with bundle sheath (BS) cell ultrastructure, leaf gas exchange, and C<sub>4</sub> pathway biochemistry in five species from the two C<sub>4</sub> clades and closely related C<sub>3</sub> genera. All species in <italic>Allionia, Okenia</italic> and <italic>Boerhavia</italic> are C<sub>4</sub>, while no C<sub>4</sub> species occur in any other genera of the family, including three that branch between <italic>Allionia</italic> and <italic>Boerhavia</italic>. This demonstrates that C<sub>4</sub> photosynthesis evolved twice in Nyctaginaceae. <italic>Boerhavia</italic> species use the NADP-malic enzyme (NADP-ME) subtype of C<sub>4</sub> photosynthesis, while <italic>Allionia</italic> species use the NAD-malic enzyme (NAD-ME) subtype. The BS cells of <italic>Allionia</italic> have many more mitochondria than the BS of <italic>Boerhavia</italic>. Bundle sheath mitochondria are closely associated with chloroplasts in <italic>Allionia</italic> which facilitates CO<sub>2</sub> refixation following decarboxylation by mitochondrial NAD-ME. The close relationship between <italic>Allionia</italic> and <italic>Boerhavia</italic> could provide insights into why NADP-ME versus NAD-ME subtypes evolve, particularly when coupled to analysis of their respective genomes. As such, the group is an excellent system to dissect the organizational hierarchy of convergent versus divergent traits produced by C<sub>4</sub> evolution, enabling us to understand when convergence is favored versus when divergent modifications can result in a common phenotype.</p>