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Variation in leaf anatomical traits relates to the evolution of C4 photosynthesis in Tribuloideae (Zygophyllaceae)

Lauterbach, Maximilian, Zimmer, Regina, Alexa, Andrea Christine, Adachi, Shunsuke, Sage, Rowan, Sage, Tammy, MacFarlane, Terry, Ludwig, Martha, Kadereit, Gudrun
Perspectives in plant ecology, evolution and systematics 2019 v.39 pp. 125463
Balanites, C3 plants, C4 photosynthesis, C4 plants, Kallstroemia, Tribulus, carbon, genetic markers, herbs, hybrids, leaves, phylogeny, stable isotopes
Tribuloideae (Zygophyllaceae, Zygophyllales) is a warm-climate clade of mostly creeping herbs with an uncertain number of C4 species from at least two genera, raising the possibility of multiple C4 origins within this lineage. To delineate C3 and C4 distributions within Tribuloideae, we conducted a phylogenetic analysis using four genetic markers from 78 accessions of Tribuloideae. δ13C values from 68 Tribuloideae members detected 42 C4 species in the genera Kallstroemia, Tribulopis and Tribulus, and no C4 in Balanites, Neoluederitzia, and Sisyndite. All Kallstroemia are C4, while Tribulopis and Tribulus include C3 species. Two independent C4 origins are supported, one in Tribulus and a second in Kallstroemia; both lineages are NADP-ME subtypes. The C4Tribulopis clade occurs in a conflicting position that suggests a hybrid origin between ancestral Kallstroemia and C3Tribulopis/Tribulus species. Anatomical assessment did not show enhanced vein density in C3 Tribuloideae, however, relative bundle sheath area is greater in C3 clades closely related to the C4 lineages, supporting a hypothesis that bundle sheath enhancement in C3 Tribuloideae facilitated C4 evolution.