CAM photosynthesis: the acid test

Abstract

There is currently considerable interest in the prospects for bioengineering crassulacean acid metabolism (CAM) photosynthesisor key elements associated with it, such as increased water-use efficiencyinto C 3 plants. Resolving how CAM photosynthesis evolved from the ancestral C 3 pathway could provide valuable insights into the targets for such bioengineering efforts. It has been proposed that the ability to accumulate organic acids at night may be common among C 3 plants, and that the transition to CAM might simply require enhancement of pre-existing fluxes, without the need for changes in circadian or diurnal regulation. We show, in a survey encompassing 40 families of vascular plants, that nocturnal acidification is a feature entirely restricted to CAM species. Although many C 3 species can synthesize malate during the light period, we argue that the switch to night-time malic acid accumulation requires a fundamental metabolic reprogramming that couples glycolytic breakdown of storage carbohydrate to the process of net dark CO 2 fixation. This central element of the CAM pathway, even when expressed at a low level, represents a biochemical capability not seen in C 3 plants, and so is better regarded as a discrete evolutionary innovation than as part of a metabolic continuum between C 3 and CAM.

Transcriptomic analysis of the C3-CAM transition in Cistanthe longiscapa, a drought tolerant plant in the Atacama Desert

“…CAM plants can be characterized by displaying a nocturnal acidification, a feature not found in C3 plants (Winter and Smith, 2022). In this study we were able to detect different levels of nocturnal leaf acidification in C. longiscapa plants collected from different sites and to associate these differences with the development of an abiotic stress response.…”

“…A fine temporal and spatial regulation of metabolites and gases flow is required in CAM to avoid futile cycles, to favor the proper metabolites storage and to overcome the obstacles imposed by the succulent CAM plants leaf architecture. However, there are still several transporters that are unknown and are key for a CAM plant operation (Winter and Smith, 2022). Among the many transporters with a differential expression at dawn in S1 plants, we found several clearly related to the CAM metabolism: Dicarboxylate transporter (DiT1) and an aluminum-activated malate transporter (ALMT1) could be involved in the export of malic acid from the vacuole at dawn (Wai et al ., 2019, Ceusters et al ., 2021).…”

“…Succulent tissues might be advantageous for CAM plants due to the possibility to maximize the acid- and water-storage capacity of its cells (Lim et al ., 2020, Winter and Smith, 2022). C. longiscapa plants from the S1 site, who would be performing CAM metabolism, displayed on average 3 times larger succulency compared to site S3 plants (Supplementary Figure 1).…”

“…CAM is a remarkable example of convergent evolution of a complex trait that has evolved independently multiple times in about 6% of species and at least 37 plant families (Winter et al ., 2020). Different types of CAM have been described (Messerschmid et al ., 2021; Winter and Smith, 2022), for instance, in obligate CAM plants, like most cacti, carbon is fixed constitutively at night in contrast to facultative CAM plants, where nocturnal fixation is induced by drought, salt stress or ontogeny (Winter K., 2019; Schiller and Bräutigam, 2021). In CAM cycling plants, carbon is fixed nocturnally from recycled respiratory CO 2 , and during the day with C3 photosynthesis (Schiller and Bräutigam, 2021).…”

“…Among the many transporters with a differential expression at dawn in S1 plants, we found several clearly related to the CAM metabolism: Dicarboxylate transporter (DiT1) and an aluminum-activated malate transporter (ALMT1) could be involved in the export of malic acid from the vacuole at dawn (Wai et al, 2019, Ceusters et al, 2021. Succulent tissues might be advantageous for CAM plants due to the possibility to maximize the acid-and water-storage capacity of its cells (Lim et al, 2020, Winter andSmith, 2022).…”