The age of the grasses and clusters of origins of C₄ photosynthesis

Abstract

At high temperatures and relatively low CO 2 concentrations, plants can most efficiently fix carbon to form carbohydrates through C 4 photosynthesis rather than through the ancestral and more widespread C 3 pathway. Because most C 4 plants are grasses, studies of the origin of C 4 are intimately tied to studies of the origin of the grasses. We present here a phylogeny of the grass family, based on nuclear and chloroplast genes, and calibrated with six fossils. We find that the earliest origins of C 4 likely occurred about 32 million years ago (Ma) in the Oligocene, coinciding with a reduction in global CO 2 levels. After the initial appearance of C 4 species, photosynthetic pathway changed at least 15 more times; we estimate nine total origins of C 4 from C 3 ancestors, at least two changes of C 4 subtype, and five reversals to C 3 . We find a cluster of C 4 to C 3 reversals in the Early Miocene correlating with a drop in global temperatures, and a subsequent cluster of C 4 origins in the Mid-Miocene, correlating with the rise in temperature at the Mid-Miocene climatic optimum. In the process of dating the origins of C 4 , we were also able to provide estimated times for other major events in grass evolution. We find that the common ancestor of the grasses (the crown node) originated in the upper Cretaceous. The common ancestor of maize and rice lived at 52 AE 8 Ma.

The Evolutionary History of Ehrhartoideae, Oryzeae, and Oryza

“…In contrast, support for the BEP clade, which includes rice, was not strong in early phylogenies (Kellogg and Linder 1995). However, the two most recent phylogenies of the grasses (Bouchenak-Khelladi et al 2008;Vicentini et al 2008) both find strong support for monophyly of the clade.…”

“…Genomic data from a variety of cereals confirm that the duplication occurred before the common ancestor of maize and rice. Data from the early diverging grasses in subfamilies Anomochlooideae, Pharoideae, and Puelioideae are more limited, but phylogenies of many individual gene families (see e.g., indicate that the duplication occurred shortly before the common ancestor of the grass family (70.9±9.2 Ma) (Vicentini et al 2008). As expected for duplicated genes, the duplicates have generally diverged in expression pattern and presumably function (Lin et al 2008;Preston and Kellogg 2007).…”

“…Within Vicentini et al (2008) estimated the divergence of Ehrhartoideae from Streptogyna at 43.1±7.2 million years ago, during the Eocene. This was a period of earth history when global climate was considerably warmer than it is now and there were no polar ice sheets (Zachos et al 2001).…”

“…Grasses are in the gray box. Relationships among grass subfamilies based on data from Vicentini et al (2008); the position of subfamily Microairoideae is unresolved within the PACCMAD clade, and is not included. Asterisk indicates a clade that is poorly supported by the available data.…”

“…A recent study places the maize-rice divergence at 51.6±7.9 million years ago (Vicentini et al 2008). This estimate is quite similar to the 50-million-year date commonly attributed to the comprehensive review of grass evolution provided by Gaut (2002), who based the date in turn on a citation from Stebbins (1981).…”