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

Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu; Jenkins, Jerry; Shu, Shengqiang; Tang, Haibao; Liu, Degao; Weighill, Deborah A.; Yim, Won Cheol; Ha, Jungmin; Heyduk, Karolina; Goodstein, David M.; Guo, Hao -Bo; Moseley, Robert C.; Fitzek, Elisabeth; Jawdy, Sara; Zhang, Zhihao; Xie, Meng; Hartwell, James; Grimwood, Jane; Abraham, Paul E.; Mewalal, Ritesh; Beltran, Juan D.; Boxall, Susanna F.; Dever, Louisa V.; Palla, Kaitlin J.; Albion, Rebecca; Garcia, Travis; Mayer, Jesse A.; Lim, Sung Don; Wai, Ching Man; Peluso, Paul; Van Buren, Robert; De Paoli, Henrique Cestari; Borland, Anne M.; Guo, Hong; Chen, Jin -Gui; Muchero, Wellington; Yin, Yanbin; Jacobson, Daniel A.; Tschaplinski, Timothy J.; Hettich, Robert L.; Ming, Ray; Winter, Klaus; Leebens-Mack, James H.; Smith, J. Andrew C.; Cushman, John C.; Schmutz, Jeremy; Tuskan, Gerald A.

doi:10.1038/s41467-017-01491-7

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

Journal Article · Fri Dec 01 00:00:00 EST 2017 · Nature Communications

DOI:https://doi.org/10.1038/s41467-017-01491-7· OSTI ID:1413629

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^[2]; Jenkins, Jerry ^[3]; Shu, Shengqiang ^[4];

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^[6]; Ha, Jungmin ^[6]; Heyduk, Karolina ^[7]; Goodstein, David M. ^[4]; Guo, Hao -Bo ^[8]; Moseley, Robert C. ^[1]; Fitzek, Elisabeth ^[9]; Jawdy, Sara ^[2]; Zhang, Zhihao ^[2];

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^[10]; Grimwood, Jane ^[3] more »

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Fujian Agriculture and Forestry Univ., Fujian (China)
Univ. of Nevada, Reno, NV (United States)
Univ. of Georgia, Athens, GA (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Northern Illinois Univ., DeKalb, IL (United States)
Univ. of Liverpool, Liverpool (United Kingdom)
Univ. of Oxford, Oxford (United Kingdom)
Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Pacific Biosciences, Inc., Menlo Park, CA (United States)
Michigan State Univ., East Lansing, MI (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Newcastle Univ., Newcastle upon Tyne (United Kingdom)
Fujian Agriculture and Forestry Univ., Fujian (China); Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Smithsonian Tropical Research Institute, Ancon (Republic of Panama)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1413629

Alternate ID(s):: OSTI ID: 1435095

Journal Information:: Nature Communications, Vol. 8, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 96 works

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References (81)

An innovative platform for quick and flexible joining of assorted DNA fragments De Paoli, Henrique Cestari; Tuskan, Gerald A.; Yang, Xiaohan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19278	journal	January 2016
Orchestration of carbohydrate processing for crassulacean acid metabolism Borland, Anne M.; Guo, Hao-Bo; Yang, Xiaohan Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.04.001	journal	June 2016
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands Borland, A. M.; Griffiths, H.; Hartwell, J. Journal of Experimental Botany, Vol. 60, Issue 10 https://doi.org/10.1093/jxb/erp118	journal	April 2009
Karyotype and Gene Order Evolution from Reconstructed Extinct Ancestors Highlight Contrasts in Genome Plasticity of Modern Rosid Crops Murat, Florent; Zhang, Rongzhi; Guizard, Sébastien Genome Biology and Evolution, Vol. 7, Issue 3 https://doi.org/10.1093/gbe/evv014	journal	January 2015
Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets Zeng, Liping; Zhang, Ning; Zhang, Qiang Wiley-Blackwell Publishing, Inc. https://doi.org/10.5167/uzh-136213	text	January 2017
phot1 and phot2 mediate blue light regulation of stomatal opening Kinoshita, Toshinori; Doi, Michio; Suetsugu, Noriyuki Nature, Vol. 414, Issue 6864 https://doi.org/10.1038/414656a	journal	December 2001
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Gene tree discordance, phylogenetic inference and the multispecies coalescent Degnan, James H.; Rosenberg, Noah A. Trends in Ecology & Evolution, Vol. 24, Issue 6 https://doi.org/10.1016/j.tree.2009.01.009	journal	June 2009
Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. Puente, P.; Wei, N.; Deng, X. W. The EMBO Journal, Vol. 15, Issue 14 https://doi.org/10.1002/j.1460-2075.1996.tb00743.x	journal	July 1996
PlantCAZyme: a database for plant carbohydrate-active enzymes Ekstrom, Alexander; Taujale, Rahil; McGinn, Nathan Database, Vol. 2014 https://doi.org/10.1093/database/bau079	journal	January 2014
Wheels within wheels: the plant circadian system Hsu, Polly Yingshan; Harmer, Stacey L. Trends in Plant Science, Vol. 19, Issue 4 https://doi.org/10.1016/j.tplants.2013.11.007	journal	April 2014
The regulation of phosphoenolpyruvate carboxylase in CAM plants Nimmo, Hugh G. Trends in Plant Science, Vol. 5, Issue 2 https://doi.org/10.1016/S1360-1385(99)01543-5	journal	February 2000
Photosynthetic Response and Adaptation to Temperature in Higher Plants Berry, J.; Bjorkman, O. Annual Review of Plant Physiology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pp.31.060180.002423	journal	June 1980
Molecular interaction of bZIP domains of GBF1, HY5 and HYH inArabidopsisseedling development Ram, Hathi; Chattopadhyay, Sudip Plant Signaling & Behavior, Vol. 8, Issue 1 https://doi.org/10.4161/psb.22703	journal	January 2013
Biogeography of the ecosystems of the healthy human body Zhou, Yanjiao; Gao, Hongyu; Mihindukulasuriya, Kathie A. Genome Biology, Vol. 14, Issue 1 https://doi.org/10.1186/gb-2013-14-1-r1	journal	January 2013
Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana Xiang, Li; Le Roy, Katrien; Bolouri-Moghaddam, Mohammad-Reza Journal of Experimental Botany, Vol. 62, Issue 11 https://doi.org/10.1093/jxb/err069	journal	March 2011
Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution Wake, D. B.; Wake, M. H.; Specht, C. D. Science, Vol. 331, Issue 6020 https://doi.org/10.1126/science.1188545	journal	February 2011
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas Rai, Aditi; Bhattacharjee, Arindam Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02278-7	journal	April 2021
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks Trapnell, Cole; Roberts, Adam; Goff, Loyal Nature Protocols, Vol. 7, Issue 3 https://doi.org/10.1038/nprot.2012.016	journal	March 2012
A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress Wang, Guodong; Kong, Fanying; Zhang, Song Journal of Experimental Botany, Vol. 66, Issue 11 https://doi.org/10.1093/jxb/erv102	journal	March 2015
A Minimal Serine/Threonine Protein Kinase Circadianly Regulates Phospho enol pyruvate Carboxylase Activity in Crassulacean Acid Metabolism-Induced Leaves of the Common Ice Plant Taybi, Tahar; Patil, Shameekumar; Chollet, Raymond Plant Physiology, Vol. 123, Issue 4 https://doi.org/10.1104/pp.123.4.1471	journal	August 2000
Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres Paterson, Andrew H.; Wendel, Jonathan F.; Gundlach, Heidrun Nature, Vol. 492, Issue 7429 https://doi.org/10.1038/nature11798	journal	December 2012
Convergent evolution of the genomes of marine mammals Foote, Andrew D.; Liu, Yue; Thomas, Gregg W. C. Nature Genetics, Vol. 47, Issue 3 https://doi.org/10.1038/ng.3198	journal	January 2015
The pineapple genome and the evolution of CAM photosynthesis Ming, Ray; VanBuren, Robert; Wai, Ching Man Nature Genetics, Vol. 47, Issue 12 https://doi.org/10.1038/ng.3435	journal	November 2015
Genome Sequencing of Kocuria varians Strain 80, Isolated from Starter Culture for Dry Sausage Konorov, Evgenii A.; Kurbakov, Konstantin A.; Minaev, Mikhail Y. Microbiology Resource Announcements, Vol. 10, Issue 8 https://doi.org/10.1128/mra.00086-21	journal	February 2021
The Law of Parsimony Laird, John Monist, Vol. 29, Issue 3 https://doi.org/10.5840/monist191929317	journal	January 1919
Engineering crassulacean acid metabolism to improve water-use efficiency Borland, Anne M.; Hartwell, James; Weston, David J. Trends in Plant Science, Vol. 19, Issue 5 https://doi.org/10.1016/j.tplants.2014.01.006	journal	May 2014
The I-TASSER Suite: protein structure and function prediction Yang, Jianyi; Yan, Renxiang; Roy, Ambrish Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3213	journal	December 2014
Nicotinamide Adenine Dinucleotide-specific “Malic” Enzyme in Kalanchoë daigremontiana and Other Plants Exhibiting Crassulacean Acid Metabolism Dittrich, Peter Plant Physiology, Vol. 57, Issue 2 https://doi.org/10.1104/pp.57.2.310	journal	February 1976
Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars Fujiki, Yuki; Yoshikawa, Yoko; Sato, Tokuyuki Physiologia Plantarum, Vol. 111, Issue 3 https://doi.org/10.1034/j.1399-3054.2001.1110312.x	journal	March 2001
Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice Nijhawan, Aashima; Jain, Mukesh; Tyagi, Akhilesh K. Plant Physiology, Vol. 146, Issue 2 https://doi.org/10.1104/pp.107.112821	journal	December 2007
Protection by light against heat stress in leaves of tropical crassulacean acid metabolism plants containing high acid levels Krause, G. Heinrich; Winter, Klaus; Krause, Barbara Functional Plant Biology, Vol. 43, Issue 11 https://doi.org/10.1071/FP16093	journal	January 2016
Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition Chen, Xiangbin; Yao, Qinfang; Gao, Xiuhua Current Biology, Vol. 26, Issue 5 https://doi.org/10.1016/j.cub.2015.12.066	journal	March 2016
Analysis of the function of two circadian-regulated CONSTANS-LIKE genes: Analysis of Arabidopsis CONSTANS-LIKE genes Ledger, Susan; Strayer, Carl; Ashton, Fern The Plant Journal, Vol. 26, Issue 1 https://doi.org/10.1046/j.1365-313x.2001.01003.x	journal	April 2001
Crassulacean acid metabolism photosynthesis: `working the night shift' Black, Clanton C.; Osmond, C. Barry Photosynthesis Research, Vol. 76, Issue 1/3, p. 329-341 https://doi.org/10.1023/A:1024978220193	journal	April 2003
Convergent transcriptional specializations in the brains of humans and song-learning birds Pfenning, A. R.; Hara, E.; Whitney, O. Science, Vol. 346, Issue 6215 https://doi.org/10.1126/science.1256846	journal	December 2014
The genome sequence of the orchid Phalaenopsis equestris Cai, Jing; Liu, Xin; Vanneste, Kevin Nature Genetics, Vol. 47, Issue 1 https://doi.org/10.1038/ng.3149	journal	November 2014
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism Hartwell, James; Dever, Louisa V.; Boxall, Susanna F. Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.03.019	journal	June 2016
Novel thioether bond revealed by a 1.7 Å crystal structure of galactose oxidase Ito, Nobutoshi; Phillips, Simon E. V.; Stevens, Conrad Nature, Vol. 350, Issue 6313 https://doi.org/10.1038/350087a0	journal	March 1991
Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas Hu, Yibo; Wu, Qi; Ma, Shuai Proceedings of the National Academy of Sciences, Vol. 114, Issue 5 https://doi.org/10.1073/pnas.1613870114	journal	January 2017
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots Moore, M. J.; Soltis, P. S.; Bell, C. D. Proceedings of the National Academy of Sciences, Vol. 107, Issue 10 https://doi.org/10.1073/pnas.0907801107	journal	February 2010
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla Nature, Vol. 449, Issue 7161, p. 463-467 https://doi.org/10.1038/nature06148	journal	August 2007
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana Plant Physiology, Vol. 167, Issue 1 https://doi.org/10.1104/pp.114.251827	journal	November 2014
Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response Wang, Wangxia; Vinocur, Basia; Shoseyov, Oded Trends in Plant Science, Vol. 9, Issue 5 https://doi.org/10.1016/j.tplants.2004.03.006	journal	May 2004
PosiGene: automated and easy-to-use pipeline for genome-wide detection of positively selected genes Sahm, Arne; Bens, Martin; Platzer, Matthias Nucleic Acids Research, Vol. 45, Issue 11 https://doi.org/10.1093/nar/gkx179	journal	March 2017
Resolving the Activation Site of Positive Regulators in Plant Phosphoenolpyruvate Carboxylase Schlieper, Daniel; Förster, Kerstin; Paulus, Judith K. Molecular Plant, Vol. 7, Issue 2 https://doi.org/10.1093/mp/sst130	journal	February 2014
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis Mockler, T. C.; Michael, T. P.; Priest, H. D. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 72, Issue 1 https://doi.org/10.1101/sqb.2007.72.006	journal	January 2007
Convergent Evolution and the Origin of Complex Phenotypes in the Age of Systems Biology Washburn, Jacob D.; Bird, Kevin A.; Conant, Gavin C. International Journal of Plant Sciences, Vol. 177, Issue 4 https://doi.org/10.1086/686009	journal	May 2016
Development and use of bioenergy feedstocks for semi-arid and arid lands Cushman, John C.; Davis, Sarah C.; Yang, Xiaohan Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv087	journal	April 2015
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
Coupled chaperone action in folding and assembly of hexadecameric Rubisco Liu, Cuimin; Young, Anna L.; Starling-Windhof, Amanda Nature, Vol. 463, Issue 7278 https://doi.org/10.1038/nature08651	journal	January 2010
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression Hartwell, James; Gill, Aideen; Nimmo, Gillian A. The Plant Journal, Vol. 20, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.t01-1-00609.x	journal	November 1999
Crassulacean acid metabolism photosynthesis: ‘working the night shift’ Black, Clanton C.; Barry Osmond, C. Discoveries in Photosynthesis https://doi.org/10.1007/1-4020-3324-9_79	book	January 2005
High-throughput functional annotation and data mining with the Blast2GO suite Gotz, S.; Garcia-Gomez, J. M.; Terol, J. Nucleic Acids Research, Vol. 36, Issue 10 https://doi.org/10.1093/nar/gkn176	journal	April 2008
Continuous evolution of base editors with expanded target compatibility and improved activity Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M. Nature Biotechnology, Vol. 37, Issue 9 https://doi.org/10.1038/s41587-019-0193-0	journal	July 2019
Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism Holtum, Joseph A. M.; Smith, J. Andrew C.; Neuhaus, H. Ekkehard Functional Plant Biology, Vol. 32, Issue 5 https://doi.org/10.1071/FP04189	journal	January 2005
Inferring Phylogeny Despite Incomplete Lineage Sorting Maddison, Wayne P.; Knowles, L. Lacey Systematic Biology, Vol. 55, Issue 1 https://doi.org/10.1080/10635150500354928	journal	February 2006
The Amborella Genome and the Evolution of Flowering Plants Albert, V. A.; Barbazuk, W. B.; dePamphilis, C. W. Science, Vol. 342, Issue 6165 https://doi.org/10.1126/science.1241089	journal	December 2013
Mechanism for deactivation of Rubisco under moderate heat stress Salvucci, Michael E.; Crafts-Brandner, Steven J. Physiologia Plantarum, Vol. 122, Issue 4 https://doi.org/10.1111/j.1399-3054.2004.00419.x	journal	December 2004
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes Mirarab, Siavash; Warnow, Tandy Bioinformatics, Vol. 31, Issue 12 https://doi.org/10.1093/bioinformatics/btv234	journal	June 2015
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research Conesa, A.; Gotz, S.; Garcia-Gomez, J. M. Bioinformatics, Vol. 21, Issue 18 https://doi.org/10.1093/bioinformatics/bti610	journal	August 2005
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway Zhang, Liangsheng; Chen, Fei; Zhang, Guo-Qiang The Plant Journal, Vol. 86, Issue 2 https://doi.org/10.1111/tpj.13159	journal	April 2016
Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets Zeng, Liping; Zhang, Ning; Zhang, Qiang New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14503	journal	March 2017
Photosynthesis, Reorganized West-Eberhard, M. J.; Smith, J. A. C.; Winter, K. Science, Vol. 332, Issue 6027 https://doi.org/10.1126/science.1205336	journal	April 2011
A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases Owen, Nick A.; Griffiths, Howard New Phytologist, Vol. 200, Issue 4 https://doi.org/10.1111/nph.12461	journal	August 2013
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world Yang, Xiaohan; Cushman, John C.; Borland, Anne M. New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13393	journal	July 2015
Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads Kajitani, Rei; Toshimoto, Kouta; Noguchi, Hideki Genome Research, Vol. 24, Issue 8 https://doi.org/10.1101/gr.170720.113	journal	April 2014
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist Parisi, Giulia; Saco, Justin D.; Salazar, Felix B. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-12901-3	journal	January 2020
Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis Rokitta, Sebastian D.; Von Dassow, Peter; Rost, Björn BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-1051	journal	January 2014
Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification Christopher, J. T.; Holtum, Jam. Plant Physiology, Vol. 112, Issue 1 https://doi.org/10.1104/pp.112.1.393	journal	September 1996
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research Liu, Degao; Hu, Rongbin; Palla, Kaitlin J. Current Opinion in Plant Biology, Vol. 30 https://doi.org/10.1016/j.pbi.2016.01.007	journal	April 2016
A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity Magallón, Susana; Gómez‐Acevedo, Sandra; Sánchez‐Reyes, Luna L. New Phytologist, Vol. 207, Issue 2 https://doi.org/10.1111/nph.13264	journal	December 2014
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach Soltis, D. E.; Mort, M. E.; Latvis, M. American Journal of Botany, Vol. 100, Issue 5 https://doi.org/10.3732/ajb.1300044	journal	April 2013
Evolution along the crassulacean acid metabolism continuum Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark Functional Plant Biology, Vol. 37, Issue 11 https://doi.org/10.1071/FP10084	journal	January 2010
Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate Martins, Marina Camara Mattos; Hejazi, Mahdi; Fettke, Joerg Plant Physiology, Vol. 163, Issue 3 https://doi.org/10.1104/pp.113.226787	journal	September 2013
Predictable convergence in hemoglobin function has unpredictable molecular underpinnings Natarajan, Chandrasekhar; Hoffmann, Federico G.; Weber, Roy E. Science, Vol. 354, Issue 6310 https://doi.org/10.1126/science.aaf9070	journal	October 2016
Genetic basis for the establishment of endosymbiosis in Paramecium He, Ming; Wang, Jinfeng; Fan, Xinpeng The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-018-0341-4	journal	January 2019

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Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave Yin, Hengfu; Guo, Hao-Bo; Weston, David J. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4964-7	journal	August 2018
Comparative Genomics Analysis Provides New Insight Into Molecular Basis of Stomatal Movement in Kalanchoë fedtschenkoi Moseley, Robert C.; Tuskan, Gerald A.; Yang, Xiaohan Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00292	journal	March 2019
Phylogenomic Analysis of the PEBP Gene Family from Kalanchoë Mackenzie, Kathryn Kuligowska; Coelho, Lívia Lopes; Lütken, Henrik Agronomy, Vol. 9, Issue 4 https://doi.org/10.3390/agronomy9040171	journal	March 2019
Ecophysiology of constitutive and facultative CAM photosynthesis Winter, Klaus Journal of Experimental Botany, Vol. 70, Issue 22 https://doi.org/10.1093/jxb/erz002	journal	February 2019
Inference of Gene Regulatory Network Uncovers the Linkage between Circadian Clock and Crassulacean Acid Metabolism in Kalanchoë fedtschenkoi Moseley, Robert C.; Motta, Francis; Tuskan, Gerald A. Cells, Vol. 10, Issue 9 https://doi.org/10.3390/cells10092217	journal	August 2021
The role of cis-elements in the evolution of crassulacean acid metabolism photosynthesis Chen, Li-Yu; Xin, Yinghui; Wai, Ching Man Horticulture Research, Vol. 7, Issue 1 https://doi.org/10.1038/s41438-019-0229-0	journal	January 2020
Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism Zhang, Jin; Hu, Rongbin; Sreedasyam, Avinash GigaScience, Vol. 9, Issue 3 https://doi.org/10.1093/gigascience/giaa018	journal	March 2020
Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses Wang, Xiyin; Gowik, Udo; Tang, Haibao Genome Biology, Vol. 10, Issue 6 https://doi.org/10.1186/gb-2009-10-6-r68	journal	January 2009
Genome-wide phylogenetic and structural analysis reveals the molecular evolution of the ABA receptor gene family Yang, Jing-Fang; Chen, Mo-Xian; Zhang, Jian-Hua Journal of Experimental Botany, Vol. 71, Issue 4 https://doi.org/10.1093/jxb/erz511	journal	November 2019
Contingency and determinism in evolution: Replaying life’s tape Blount, Zachary D.; Lenski, Richard E.; Losos, Jonathan B. Science, Vol. 362, Issue 6415 https://doi.org/10.1126/science.aam5979	journal	November 2018
A review of the cytotaxonomy of Kalanchoe (Crassulaceae subfam. Kalanchooideae) with reference to evolutionary trends in the genus Smith, Gideon F. Phytotaxa, Vol. 560, Issue 2 https://doi.org/10.11646/phytotaxa.560.2.2	journal	September 2022
Agave angustifolia albino plantlets lose stomatal physiology function by changing the development of the stomatal complex due to a molecular disruption Sara, Hernández-Castellano; René, Garruña-Hernández; Rosa, Us-Camas Molecular Genetics and Genomics, Vol. 295, Issue 3 https://doi.org/10.1007/s00438-019-01643-y	journal	January 2020
RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum Zou, Long-Hai; Wan, Xiao; Deng, Hua Scientific Data, Vol. 5, Issue 1 https://doi.org/10.1038/sdata.2018.252	journal	November 2018

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