Independent and Parallel Recruitment of Preexisting Mechanisms Underlying C ₄ Photosynthesis

Abstract

C₄ photosynthesis allows increased photosynthetic efficiency because carbon dioxide (CO₂) is concentrated around the key enzyme RuBisCO. Leaves of C₄ plants exhibit modified biochemistry, cell biology, and leaf development, but despite this complexity, C₄ photosynthesis has evolved independently in at least 45 lineages of plants. We found that two independent lineages of C₄ plant, whose last common ancestor predates the divergence of monocotyledons and dicotyledons about 180 million years ago, show conserved mechanisms controlling the expression of genes important for release of CO(2) around RuBisCO in bundle sheath (BS) cells. Orthologous genes from monocotyledonous and dicotyledonous C₃ species also contained conserved regulatory elements that conferred BS specificity when placed into C₄ species. We conclude that these conserved functional genetic elements likely facilitated the repeated evolution of C₄ photosynthesis.

Anatomical enablers and the evolution of C 4 photosynthesis in grasses

“…Once a photorespiratory pump is fixed by natural selection, the biochemical components of the C 4 pathway can be gradually acquired and optimized until a highly efficient C 4 trait emerges. All enzymes of the C 4 pathway already exist in C 3 plants, and C 4 compatible promoter sequences are widespread in angiosperms (6,7). The evolution of the C 4 trait can consequently require relatively few mutations in plants with a suitable leaf anatomy, which, in grasses, largely includes members of the PACMAD clade (Fig.…”

“…Despite this complexity, it evolved more than 62 times independently in distantly related groups of flowering plants (5). These recurrent C 4 origins were probably facilitated by the existence in most C 3 plants of metabolic modules that are suitable for the C 4 pathway and can be recruited for this function through relatively few mutations (6,7). In addition, the photorespiratory pump based on glycine decarboxylase is a likely evolutionary stable intermediate phenotype on the road from C 3 to C 4 (3,8).…”

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO 2 ]

“…The fact that C 4 photosynthesis has independently evolved in many genetic backgrounds on different occasions increases the likelihood that successful engineering can be achieved [107]. Specific evidence for this assertion includes that: (i) independent lineages of C 4 species share common mechanisms controlling the localization of key enzymes for C 4 photosynthesis in bundle sheath cells; and (ii) specific localization of enzymes in C 4 leaves to bundle sheath versus mesophyll cells can be achieved by modification of trans-factors without a change in existing cis-regulation of C 3 species [124].…”

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…However, it is now clear that multiple genes are expressed preferentially in M or BS cells of C 4 G. gynandra because of pre-existing cis-elements located in orthologous genes from A. thaliana. For example, both genes encoding the heterodimeric NAD-ME in G. gynandra contain elements in the coding sequence that determine BS expression, and these elements are found in the orthologues from A. thaliana [73,74]. The genes from A. thaliana are not preferentially expressed in the BS in the ancestral C 3 state, but they are when placed into leaves of C 4 G. gynandra.…”