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

ABSTRACT: 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 Kalanchoë 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.

SUBMITTER: Yang X

PROVIDER: S-EPMC5711932 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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

Yang Xiaohan X Hu Rongbin R Yin Hengfu H Jenkins Jerry J Shu Shengqiang S Tang Haibao H Liu Degao D Weighill Deborah A DA Cheol Yim Won W Ha Jungmin J Heyduk Karolina K Goodstein David M DM Guo Hao-Bo HB Moseley Robert C RC Fitzek Elisabeth E Jawdy Sara S Zhang Zhihao Z Xie Meng M Hartwell James J Grimwood Jane J Abraham Paul E PE Mewalal Ritesh R Beltrán Juan D JD Boxall Susanna F SF Dever Louisa V LV Palla Kaitlin J KJ Albion Rebecca R Garcia Travis T Mayer Jesse A JA Don Lim Sung S Man Wai Ching C Peluso Paul P Van Buren Robert R De Paoli Henrique Cestari HC Borland Anne M AM Guo Hong H Chen Jin-Gui JG Muchero Wellington W Yin Yanbin Y Jacobson Daniel A DA Tschaplinski Timothy J TJ Hettich Robert L RL Ming Ray R Winter Klaus K Leebens-Mack James H JH Smith J Andrew C JAC Cushman John C JC Schmutz Jeremy J Tuskan Gerald A GA

Nature communications 20171201 1

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 C<sub>3</sub> photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species w ...[more]

PMID: 29196618

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Project description:BACKGROUND:Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. RESULTS:Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 ?mol m-2 s-1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 ?mol m-2 s-1) of white light to a high light treatment (1,000 ?mol m-2 s-1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. CONCLUSIONS:This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.

Dataset Information

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

Publications

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

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