Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ρ duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

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The pineapple genome and the evolution of CAM photosynthesis

Water use efficiency (WUE) is defined as the amount of carbon assimilated as biomass or grain produced per unit of water used by the crop. One of the primary questions being asked is how plants will respond to a changing climate with changes in temperature, precipitation, and carbon dioxide (CO2) that affect their WUE At the leaf level, increasing CO2 increases WUE until the leaf is exposed to temperatures exceeded the optimum for growth (i.e., heat stress) and then WUE begins to decline. Leaves subjected to water deficits (i.e., drought stress) show varying responses in WUE. The response of WUE at the leaf level is directly related to the physiological processes controlling the gradients of CO2 and H2O, e.g., leaf:air vapor pressure deficits, between the leaf and air surrounding the leaf. There a variety of methods available to screen genetic material for enhanced WUE under scenarios of climate change. When we extend from the leaf to the canopy, then the dynamics of crop water use and biomass accumulation have to consider soil water evaporation rate, transpiration from the leaves, and the growth pattern of the crop. Enhancing WUE at the canopy level can be achieved by adopting practices that reduce the soil water evaporation component and divert more water into transpiration which can be through crop residue management, mulching, row spacing, and irrigation. Climate change will affect plant growth, but we have opportunities to enhance WUE through crop selection and cultural practices to offset the impact of a changing climate.

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Water-Use Efficiency: Advances and Challenges in a Changing Climate

Drought stress, which causes a decline in quality and quantity of crop yields, has become more accentuated these days due to climatic change. Serious measures need to be taken to increase the tolerance of crop plants to acute drought conditions likely to occur due to global warming. Drought stress causes many physiological and biochemical changes in plants, rendering the maintenance of osmotic adjustment highly crucial. The degree of plant resistance to drought varies with plant species and cultivars, phenological stages of the plant, and the duration of plant exposure to the stress. Osmoregulation in plants under low water potential relies on synthesis and accumulation of osmoprotectants or osmolytes such as soluble proteins, sugars, and sugar alcohols, quaternary ammonium compounds, and amino acids, like proline. This review highlights the role of osmolytes in water-stressed plants and of enzymes entailed in their metabolism. It will be useful, especially for researchers working on the development of drought-resistant crops by using the metabolic-engineering techniques.

Osmoregulation and its actions during the drought stress in plants

Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoe fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.

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The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

The key components of crassulacean acid metabolism (CAM) - nocturnal fixation of atmospheric CO2 and its processing via Rubisco in the subsequent light period - are now reasonably well understood in terms of the biochemical reactions defining this water-saving mode of carbon assimilation. Phenotypically, however, the degree to which plants engage in the CAM cycle relative to regular C3 photosynthesis is highly variable. Depending upon species, ontogeny and environment, the contribution of nocturnal CO2 fixation to 24-h carbon gain can range continuously from close to 0% to 100%. Nevertheless, not all possible combinations of light and dark CO2 fixation appear equally common. Large-scale surveys of carbon-isotope ratios typically show a strongly bimodal frequency distribution, with relatively few intermediate values. Recent research has revealed that many species capable of low-level CAM activity are nested within the peak of C3 -type isotope signatures. While questions remain concerning the adaptive significance of dark CO2 fixation in such species, plants with low-level CAM should prove valuable models for investigating the discrete changes in genetic architecture and gene expression that have enabled the evolutionary transition from C3 to CAM.

Crassulacean acid metabolism: a continuous or discrete trait?

Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that features nocturnal CO2 uptake, facilitates increased water-use efficiency (WUE), and enables CAM plants to inhabit water-limited environments such as semi-arid deserts or seasonally dry forests. Human population growth and global climate change now present challenges for agricultural production systems to increase food, feed, forage, fiber, and fuel production. One approach to meet these challenges is to increase reliance on CAM crops, such as Agave and Opuntia, for biomass production on semi-arid, abandoned, marginal, or degraded agricultural lands. Major research efforts are now underway to assess the productivity of CAM crop species and to harness the WUE of CAM by engineering this pathway into existing food, feed, and bioenergy crops. An improved understanding of CAM has potential for high returns on research investment. To exploit the potential of CAM crops and CAM bioengineering, it will be necessary to elucidate the evolution, genomic features, and regulatory mechanisms of CAM. Field trials and predictive models will be required to assess the productivity of CAM crops, while new synthetic biology approaches need to be developed for CAM engineering. Infrastructure will be needed for CAM model systems, field trials, mutant collections, and data management.

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Erin Casey

Papers

A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world.