The cacti are one of the most celebrated radiations of succulent plants. There has been much speculation about their age, but progress in dating cactus origins has been hindered by the lack of fossil data for cacti or their close relatives. Using a hybrid phylogenomic approach, we estimated that the cactus lineage diverged from its closest relatives ≈35 million years ago (Ma). However, major diversification events in cacti were more recent, with most species-rich clades originating in the late Miocene, ≈10-5 Ma. Diversification rates of several cactus lineages rival other estimates of extremely rapid speciation in plants. Major cactus radiations were contemporaneous with those of South African ice plants and North American agaves, revealing a simultaneous diversification of several of the world's major succulent plant lineages across multiple continents. This short geological time period also harbored the majority of origins of C 4 photosynthesis and the global rise of C 4 grasslands. A global expansion of arid environments during this time could have provided new ecological opportunity for both succulent and C 4 plant syndromes. Alternatively, recent work has identified a substantial decline in atmospheric CO 2 ≈15-8 Ma, which would have strongly favored C 4 evolution and expansion of C 4 -dominated grasslands. Lowered atmospheric CO 2 would also substantially exacerbate plant water stress in marginally arid environments, providing preadapted succulent plants with a sharp advantage in a broader set of ecological conditions and promoting their rapid diversification across the landscape.climate change | paleobotany | CAM photosynthesis P lants are generally classified as succulent when they exhibit pronounced water storage in one or more organs. High degrees of succulence are most often associated with a suite of other characteristics that together confer survival in water-limited environments. This "succulent syndrome" usually includes a shallow root system that permits rapid uptake of unpredictable precipitation; a thick, waxy cuticle that prevents excessive water loss; and Crassulacean acid metabolism (CAM), an alternative photosynthetic pathway that allows plants to uptake atmospheric CO 2 at night when water loss is minimized (1). Although some 30 plant lineages have been classified as succulent, only a small subset of those are species-rich and ecologically important elements of arid and semiarid ecosystems worldwide. These lineages include the ice plants (Aizoaceae, ≈2,000 spp), the spurges (Euphorbia, ≈2,100 spp., ≈650 of which are succulent), the stonecrops (Crassulaceae, ≈1,400 spp.), the aloes (Aloe, ≈400 spp.), the agaves (Agave, ≈200 spp.), the stapeliads and asclepiads (Apocynaceae-Asclepiadoideae, ≈3,700 spp., ≈1,150 of which are succulent) and especially the cacti (Cactaceae, ≈1,850 spp.) (2).The cacti represent the most spectacular New World radiation of succulent plants. Most cacti exhibit a highly specialized life form, with extremely succulent, photosynthetic stems and leaves that have been mo...

Using isotopic screens, phylogenetic assessments, and 45 years of physiological data, it is now possible to identify most of the evolutionary lineages expressing the C(4) photosynthetic pathway. Here, 62 recognizable lineages of C(4) photosynthesis are listed. Thirty-six lineages (60%) occur in the eudicots. Monocots account for 26 lineages, with a minimum of 18 lineages being present in the grass family and six in the sedge family. Species exhibiting the C(3)-C(4) intermediate type of photosynthesis correspond to 21 lineages. Of these, 9 are not immediately associated with any C(4) lineage, indicating that they did not share common C(3)-C(4) ancestors with C(4) species and are instead an independent line. The geographic centre of origin for 47 of the lineages could be estimated. These centres tend to cluster in areas corresponding to what are now arid to semi-arid regions of southwestern North America, south-central South America, central Asia, northeastern and southern Africa, and inland Australia. With 62 independent lineages, C(4) photosynthesis has to be considered one of the most convergent of the complex evolutionary phenomena on planet Earth, and is thus an outstanding system to study the mechanisms of evolutionary adaptation.

C4 photosynthesis is an adaptation derived from the more common C3 photosynthetic pathway that confers a higher productivity under warm temperature and low atmospheric CO2 concentration [1, 2]. C4 evolution has been seen as a consequence of past atmospheric CO2 decline, such as the abrupt CO2 fall 32-25 million years ago (Mya) [3-6]. This relationship has never been tested rigorously, mainly because of a lack of accurate estimates of divergence times for the different C4 lineages [3]. In this study, we inferred a large phylogenetic tree for the grass family and estimated, through Bayesian molecular dating, the ages of the 17 to 18 independent grass C4 lineages. The first transition from C3 to C4 photosynthesis occurred in the Chloridoideae subfamily, 32.0-25.0 Mya. The link between CO2 decrease and transition to C4 photosynthesis was tested by a novel maximum likelihood approach. We showed that the model incorporating the atmospheric CO2 levels was significantly better than the null model, supporting the importance of CO2 decline on C4 photosynthesis evolvability. This finding is relevant for understanding the origin of C4 photosynthesis in grasses, which is one of the most successful ecological and evolutionary innovations in plant history.