Atmospheric CO2 decline and the timing of CAM plant evolution

Journal article

Background and Aims: CAM photosynthesis is hypothesized to have evolved in atmospheres of low CO₂ concentration in recent geological time because of its ability to concentrate CO₂ around Rubisco and boost water use efficiency relative to C₃ photosynthesis. We assess this hypothesis by compiling estimates of when CAM clades arose using phylogenetic chronograms for 73 CAM clades. We further consider evidence of how atmospheric CO₂ affects CAM relative to C₃ photosynthesis.

Results: Where CAM origins can be inferred, strong CAM is estimated to have appeared in the past 30 million years in 46 of 48 examined clades, after atmospheric CO₂ had declined from high (near 800 ppm) to lower (<450 ppm) values. In turn, 21 of 25 clades containing CAM species (but where CAM origins are less certain) also arose in the past 30 million years. In these clades, CAM is probably younger than the clade origin. We found evidence for repeated weak CAM evolution during the higher CO₂ conditions before 30 million years ago, and possible strong CAM origins in the Crassulaceae during the Cretaceous period prior to atmospheric CO₂ decline. Most CAM-specific clades arose in the past 15 million years, in a similar pattern observed for origins of C₄ clades.

Conclusions: The evidence indicates strong CAM repeatedly evolved in reduced CO₂ conditions of the past 30 million years. Weaker CAM can pre-date low CO₂ and, in the Crassulaceae, strong CAM may also have arisen in water-limited microsites under relatively high CO₂. Experimental evidence from extant CAM species demonstrates that elevated CO₂ reduces the importance of nocturnal CO₂ fixation by increasing the contribution of C₃ photosynthesis to daily carbon gain. Thus, the advantage of strong CAM would be reduced in high CO₂, such that its evolution appears less likely and restricted to more extreme environments than possible in low CO₂.

Authors: Sage, RF; Gilman, IS; Smith, JAC; Silvera, K; Edwards, EJ

• Publication status: Published
• Peer review status: Peer reviewed
• Publisher: Oxford University Press
• Journal: Annals of Botany
• Volume: 132
• Issue: 4
• Pages: 753-770
• Publication date: 2023-08-29
• Acceptance date: 2023-08-28
• DOI: 10.1093/aob/mcad122
• EISSN: 1095-8290
• ISSN: 0305-7364
• Pmid: 37642245
• Language: English
• Keywords: photosynthesis; carbon dioxide; phylogeny; water; plants