DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Nature Communications
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2];  [3];  [4]; ORCiD logo [5];  [2]; ORCiD logo [1]; ORCiD logo [6];  [6];  [7];  [4];  [8];  [1];  [9];  [2];  [2]; ORCiD logo [2]; ORCiD logo [10];  [3] more »;  [2]; ORCiD logo [2];  [11];  [10];  [10];  [1];  [6];  [6];  [6];  [6];  [12];  [13];  [14]; ORCiD logo [1];  [15];  [8]; ORCiD logo [2];  [2];  [9]; ORCiD logo [1]; ORCiD logo [2];  [2];  [16];  [17];  [7];  [11];  [6];  [18];  [2] « less
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Fujian Agriculture and Forestry Univ., Fujian (China)
  6. Univ. of Nevada, Reno, NV (United States)
  7. Univ. of Georgia, Athens, GA (United States)
  8. Univ. of Tennessee, Knoxville, TN (United States)
  9. Northern Illinois Univ., DeKalb, IL (United States)
  10. Univ. of Liverpool, Liverpool (United Kingdom)
  11. Univ. of Oxford, Oxford (United Kingdom)
  12. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
  13. Pacific Biosciences, Inc., Menlo Park, CA (United States)
  14. Michigan State Univ., East Lansing, MI (United States)
  15. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  16. Fujian Agriculture and Forestry Univ., Fujian (China); Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
  17. Smithsonian Tropical Research Institute, Ancon (Republic of Panama)
  18. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Crassulacean acid metabolism (CAM) is a specialized photosynthetic adaptation to arid environments, found predominantly in diverse eudicotyledonous (eudicot) and monocotyledonous (monocot) lineages that diverged approximately 135 million years ago. To test whether convergent evolution underpins the independent emergences of CAM, we present de novo genome assembly and gene expression data for Kalanchoë fedtschenkoi, an obligate CAM species that was shown by multigene phylogenetic analysis to represent one of the earliest-diverging lineages of core eudicots. Our combined analysis of K. fedtschenkoi and two monocot CAM species (Ananas comosus and Phalaenopsis equestris) identified signatures of convergence in protein sequence and in the diel re-scheduling of genes involved in metabolism and signaling. Lastly, our results provide significant insight into CAM evolution, facilitating CAM-into-C3 engineering for enhancing drought tolerance in crops.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
DOE Office of Science; USDOE
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1413629
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 8; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (131)

Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. journal July 1996
Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition journal March 2016
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research journal April 2016
Orchestration of carbohydrate processing for crassulacean acid metabolism journal June 2016
Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response journal May 2004
Wheels within wheels: the plant circadian system journal April 2014
Engineering crassulacean acid metabolism to improve water-use efficiency journal May 2014
The regulation of phosphoenolpyruvate carboxylase in CAM plants journal February 2000
Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars journal March 2001
Novel thioether bond revealed by a 1.7 Å crystal structure of galactose oxidase journal March 1991
phot1 and phot2 mediate blue light regulation of stomatal opening journal December 2001
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla journal August 2007
Coupled chaperone action in folding and assembly of hexadecameric Rubisco journal January 2010
Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres journal December 2012
The genome sequence of the orchid Phalaenopsis equestris journal November 2014
Convergent evolution of the genomes of marine mammals journal January 2015
The pineapple genome and the evolution of CAM photosynthesis journal November 2015
Genetic basis for the establishment of endosymbiosis in Paramecium journal January 2019
Continuous evolution of base editors with expanded target compatibility and improved activity journal July 2019
An innovative platform for quick and flexible joining of assorted DNA fragments journal January 2016
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression journal November 1999
Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism journal January 2005
Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots journal February 2010
Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas journal January 2017
Convergent Evolution and the Origin of Complex Phenotypes in the Age of Systems Biology journal May 2016
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes journal June 2015
PlantCAZyme: a database for plant carbohydrate-active enzymes journal January 2014
Karyotype and Gene Order Evolution from Reconstructed Extinct Ancestors Highlight Contrasts in Genome Plasticity of Modern Rosid Crops journal January 2015
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands journal April 2009
Development and use of bioenergy feedstocks for semi-arid and arid lands journal April 2015
A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress journal March 2015
An efficient algorithm for large-scale detection of protein families journal April 2002
dbCAN: a web resource for automated carbohydrate-active enzyme annotation journal May 2012
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis journal January 2007
Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice journal December 2007
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth journal November 2014
A Minimal Serine/Threonine Protein Kinase Circadianly Regulates Phospho enol pyruvate Carboxylase Activity in Crassulacean Acid Metabolism-Induced Leaves of the Common Ice Plant journal August 2000
Nicotinamide Adenine Dinucleotide-specific “Malic” Enzyme in Kalanchoë daigremontiana and Other Plants Exhibiting Crassulacean Acid Metabolism journal February 1976
Mechanism for deactivation of Rubisco under moderate heat stress journal December 2004
A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases journal August 2013
A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity journal December 2014
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world journal July 2015
Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets journal March 2017
Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution journal February 2011
Photosynthetic Response and Adaptation to Temperature in Higher Plants journal June 1980
Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis journal January 2014
Biogeography of the ecosystems of the healthy human body journal January 2013
Molecular interaction of bZIP domains of GBF1, HY5 and HYH inArabidopsisseedling development journal January 2013
The Law of Parsimony journal January 1919
Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. journal July 1996
Crassulacean acid metabolism photosynthesis: ‘working the night shift’ book January 2005
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas journal April 2021
The regulation of phosphoenolpyruvate carboxylase in CAM plants journal February 2000
Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition journal March 2016
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research journal April 2016
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism journal June 2016
Orchestration of carbohydrate processing for crassulacean acid metabolism journal June 2016
Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response journal May 2004
Wheels within wheels: the plant circadian system journal April 2014
Engineering crassulacean acid metabolism to improve water-use efficiency journal May 2014
Gene tree discordance, phylogenetic inference and the multispecies coalescent journal June 2009
Crassulacean acid metabolism photosynthesis: `working the night shift' journal April 2003
Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars journal March 2001
Novel thioether bond revealed by a 1.7 Å crystal structure of galactose oxidase journal March 1991
phot1 and phot2 mediate blue light regulation of stomatal opening journal December 2001
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla journal August 2007
Coupled chaperone action in folding and assembly of hexadecameric Rubisco journal January 2010
Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres journal December 2012
The genome sequence of the orchid Phalaenopsis equestris journal November 2014
Convergent evolution of the genomes of marine mammals journal January 2015
The pineapple genome and the evolution of CAM photosynthesis journal November 2015
The I-TASSER Suite: protein structure and function prediction journal December 2014
I-TASSER: a unified platform for automated protein structure and function prediction journal March 2010
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist journal January 2020
An innovative platform for quick and flexible joining of assorted DNA fragments journal January 2016
An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II journal January 2003
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression journal November 1999
Analysis of the function of two circadian-regulated CONSTANS-LIKE genes: Analysis of Arabidopsis CONSTANS-LIKE genes journal April 2001
Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism journal January 2005
Evolution along the crassulacean acid metabolism continuum journal January 2010
Protection by light against heat stress in leaves of tropical crassulacean acid metabolism plants containing high acid levels journal January 2016
Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots journal February 2010
Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas journal January 2017
Inferring Phylogeny Despite Incomplete Lineage Sorting journal February 2006
Convergent Evolution and the Origin of Complex Phenotypes in the Age of Systems Biology journal May 2016
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research journal August 2005
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes journal June 2015
PlantCAZyme: a database for plant carbohydrate-active enzymes journal January 2014
Karyotype and Gene Order Evolution from Reconstructed Extinct Ancestors Highlight Contrasts in Genome Plasticity of Modern Rosid Crops journal January 2015
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands journal April 2009
Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana journal March 2011
Development and use of bioenergy feedstocks for semi-arid and arid lands journal April 2015
A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress journal March 2015
Resolving the Activation Site of Positive Regulators in Plant Phosphoenolpyruvate Carboxylase journal February 2014
An efficient algorithm for large-scale detection of protein families journal April 2002
High-throughput functional annotation and data mining with the Blast2GO suite journal April 2008
dbCAN: a web resource for automated carbohydrate-active enzyme annotation journal May 2012
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
PosiGene: automated and easy-to-use pipeline for genome-wide detection of positively selected genes journal March 2017
Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads journal April 2014
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis journal January 2007
Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice journal December 2007
Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification journal September 1996
Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate journal September 2013
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth journal November 2014
A Minimal Serine/Threonine Protein Kinase Circadianly Regulates Phospho enol pyruvate Carboxylase Activity in Crassulacean Acid Metabolism-Induced Leaves of the Common Ice Plant journal August 2000
Nicotinamide Adenine Dinucleotide-specific “Malic” Enzyme in Kalanchoë daigremontiana and Other Plants Exhibiting Crassulacean Acid Metabolism journal February 1976
An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV journal March 2016
Mechanism for deactivation of Rubisco under moderate heat stress journal December 2004
A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases journal August 2013
A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity journal December 2014
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world journal July 2015
Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets journal March 2017
Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway journal April 2016
Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution journal February 2011
Photosynthesis, Reorganized journal April 2011
The Amborella Genome and the Evolution of Flowering Plants journal December 2013
Convergent transcriptional specializations in the brains of humans and song-learning birds journal December 2014
Predictable convergence in hemoglobin function has unpredictable molecular underpinnings journal October 2016
Genome Sequencing of Kocuria varians Strain 80, Isolated from Starter Culture for Dry Sausage journal February 2021
Photosynthetic Response and Adaptation to Temperature in Higher Plants journal June 1980
Biogeography of the ecosystems of the healthy human body journal January 2013
Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach journal April 2013
Molecular interaction of bZIP domains of GBF1, HY5 and HYH inArabidopsisseedling development journal January 2013
Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets text January 2017
The Law of Parsimony journal January 1919
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes dataset January 2023

Cited By (27)

Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism journal March 2020
A review of the cytotaxonomy of Kalanchoe (Crassulaceae subfam. Kalanchooideae) with reference to evolutionary trends in the genus journal September 2022
Correction to: Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave journal April 2019
Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album journal June 2019
Comparative Genomics Analysis Provides New Insight Into Molecular Basis of Stomatal Movement in Kalanchoë fedtschenkoi journal March 2019
Agave angustifolia albino plantlets lose stomatal physiology function by changing the development of the stomatal complex due to a molecular disruption journal January 2020
Loss or duplication of key regulatory genes coincides with environmental adaptation of the stomatal complex in Nymphaea colorata and Kalanchoe laxiflora journal August 2018
The role of cis-elements in the evolution of crassulacean acid metabolism photosynthesis journal January 2020
RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum journal November 2018
Leaf anatomy is not correlated to CAM function in a C3+CAM hybrid species, Yucca gloriosa journal March 2020
Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism journal March 2020
Ecophysiology of constitutive and facultative CAM photosynthesis journal February 2019
Undervalued potential of crassulacean acid metabolism for current and future agricultural production journal June 2019
Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants journal September 2019
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants journal September 2019
Genome-wide phylogenetic and structural analysis reveals the molecular evolution of the ABA receptor gene family journal November 2019
Phototropins Mediate Chloroplast Movement in Phalaenopsis aphrodite (Moth Orchid) journal June 2019
On the move through time – a historical review of plant clock research journal April 2018
Contingency and determinism in evolution: Replaying life’s tape journal November 2018
Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses journal January 2009
Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave journal August 2018
The kinome of pineapple: catalog and insights into functions in crassulacean acid metabolism plants journal September 2018
Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album journal June 2019
Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae) journal January 2019
Phylogenomic Analysis of the PEBP Gene Family from Kalanchoë journal March 2019
Inference of Gene Regulatory Network Uncovers the Linkage between Circadian Clock and Crassulacean Acid Metabolism in Kalanchoë fedtschenkoi journal August 2021
Next-Generation Genome Sequencing of Sedum plumbizincicola Sheds Light on the Structural Evolution of Plastid rRNA Operon and Phylogenetic Implications within Saxifragales journal September 2019