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

Abstract

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.

Authors:
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)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1413629
Alternate Identifier(s):
OSTI ID: 1435095
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

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, and Tuskan, Gerald A. The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01491-7.
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. The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. United States. doi:10.1038/s41467-017-01491-7.
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, and Tuskan, Gerald A. Fri . "The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism". United States. doi:10.1038/s41467-017-01491-7. https://www.osti.gov/servlets/purl/1413629.
@article{osti_1413629,
title = {The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism},
author = {Yang, Xiaohan and Hu, Rongbin and Yin, Hengfu and Jenkins, Jerry and Shu, Shengqiang and Tang, Haibao and Liu, Degao and Weighill, Deborah A. and Yim, Won Cheol and Ha, Jungmin and Heyduk, Karolina and Goodstein, David M. and Guo, Hao -Bo and Moseley, Robert C. and Fitzek, Elisabeth and Jawdy, Sara and Zhang, Zhihao and Xie, Meng and Hartwell, James and Grimwood, Jane and Abraham, Paul E. and Mewalal, Ritesh and Beltran, Juan D. and Boxall, Susanna F. and Dever, Louisa V. and Palla, Kaitlin J. and Albion, Rebecca and Garcia, Travis and Mayer, Jesse A. and Lim, Sung Don and Wai, Ching Man and Peluso, Paul and Van Buren, Robert and De Paoli, Henrique Cestari and Borland, Anne M. and Guo, Hong and Chen, Jin -Gui and Muchero, Wellington and Yin, Yanbin and Jacobson, Daniel A. and Tschaplinski, Timothy J. and Hettich, Robert L. and Ming, Ray and Winter, Klaus and Leebens-Mack, James H. and Smith, J. Andrew C. and Cushman, John C. and Schmutz, Jeremy and Tuskan, Gerald A.},
abstractNote = {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.},
doi = {10.1038/s41467-017-01491-7},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {12}
}

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Works referenced in this record:

An innovative platform for quick and flexible joining of assorted DNA fragments
journal, January 2016

  • De Paoli, Henrique Cestari; Tuskan, Gerald A.; Yang, Xiaohan
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep19278

Orchestration of carbohydrate processing for crassulacean acid metabolism
journal, June 2016


Karyotype and Gene Order Evolution from Reconstructed Extinct Ancestors Highlight Contrasts in Genome Plasticity of Modern Rosid Crops
journal, January 2015

  • Murat, Florent; Zhang, Rongzhi; Guizard, Sébastien
  • Genome Biology and Evolution, Vol. 7, Issue 3
  • DOI: 10.1093/gbe/evv014

High-throughput functional annotation and data mining with the Blast2GO suite
journal, April 2008

  • Gotz, S.; Garcia-Gomez, J. M.; Terol, J.
  • Nucleic Acids Research, Vol. 36, Issue 10
  • DOI: 10.1093/nar/gkn176

Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands
journal, April 2009

  • Borland, A. M.; Griffiths, H.; Hartwell, J.
  • Journal of Experimental Botany, Vol. 60, Issue 10
  • DOI: 10.1093/jxb/erp118

phot1 and phot2 mediate blue light regulation of stomatal opening
journal, December 2001

  • Kinoshita, Toshinori; Doi, Michio; Suetsugu, Noriyuki
  • Nature, Vol. 414, Issue 6864
  • DOI: 10.1038/414656a

Convergent Evolution and the Origin of Complex Phenotypes in the Age of Systems Biology
journal, May 2016

  • Washburn, Jacob D.; Bird, Kevin A.; Conant, Gavin C.
  • International Journal of Plant Sciences, Vol. 177, Issue 4
  • DOI: 10.1086/686009

I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010

  • Roy, Ambrish; Kucukural, Alper; Zhang, Yang
  • Nature Protocols, Vol. 5, Issue 4
  • DOI: 10.1038/nprot.2010.5

Gene tree discordance, phylogenetic inference and the multispecies coalescent
journal, June 2009


A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress
journal, March 2015

  • Wang, Guodong; Kong, Fanying; Zhang, Song
  • Journal of Experimental Botany, Vol. 66, Issue 11
  • DOI: 10.1093/jxb/erv102

Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism
journal, January 2005

  • Holtum, Joseph A. M.; Smith, J. Andrew C.; Neuhaus, H. Ekkehard
  • Functional Plant Biology, Vol. 32, Issue 5
  • DOI: 10.1071/FP04189

PlantCAZyme: a database for plant carbohydrate-active enzymes
journal, January 2014


Inferring Phylogeny Despite Incomplete Lineage Sorting
journal, February 2006


The Amborella Genome and the Evolution of Flowering Plants
journal, December 2013


Wheels within wheels: the plant circadian system
journal, April 2014


The regulation of phosphoenolpyruvate carboxylase in CAM plants
journal, February 2000


Photosynthetic Response and Adaptation to Temperature in Higher Plants
journal, June 1980


Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana
journal, March 2011

  • Xiang, Li; Le Roy, Katrien; Bolouri-Moghaddam, Mohammad-Reza
  • Journal of Experimental Botany, Vol. 62, Issue 11
  • DOI: 10.1093/jxb/err069

Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution
journal, February 2011


Mechanism for deactivation of Rubisco under moderate heat stress
journal, December 2004


Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012


ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes
journal, June 2015


Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005


Convergent evolution of the genomes of marine mammals
journal, January 2015

  • Foote, Andrew D.; Liu, Yue; Thomas, Gregg W. C.
  • Nature Genetics, Vol. 47, Issue 3
  • DOI: 10.1038/ng.3198

Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres
journal, December 2012

  • Paterson, Andrew H.; Wendel, Jonathan F.; Gundlach, Heidrun
  • Nature, Vol. 492, Issue 7429
  • DOI: 10.1038/nature11798

The pineapple genome and the evolution of CAM photosynthesis
journal, November 2015

  • Ming, Ray; VanBuren, Robert; Wai, Ching Man
  • Nature Genetics, Vol. 47, Issue 12
  • DOI: 10.1038/ng.3435

dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway
journal, April 2016

  • Zhang, Liangsheng; Chen, Fei; Zhang, Guo-Qiang
  • The Plant Journal, Vol. 86, Issue 2
  • DOI: 10.1111/tpj.13159

Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014


The I-TASSER Suite: protein structure and function prediction
journal, December 2014

  • Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3213

Photosynthesis, Reorganized
journal, April 2011


A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world
journal, July 2015

  • Yang, Xiaohan; Cushman, John C.; Borland, Anne M.
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13393

Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice
journal, December 2007

  • Nijhawan, Aashima; Jain, Mukesh; Tyagi, Akhilesh K.
  • Plant Physiology, Vol. 146, Issue 2
  • DOI: 10.1104/pp.107.112821

Protection by light against heat stress in leaves of tropical crassulacean acid metabolism plants containing high acid levels
journal, January 2016

  • Krause, G. Heinrich; Winter, Klaus; Krause, Barbara
  • Functional Plant Biology, Vol. 43, Issue 11
  • DOI: 10.1071/FP16093

Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition
journal, March 2016


Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads
journal, April 2014

  • Kajitani, Rei; Toshimoto, Kouta; Noguchi, Hideki
  • Genome Research, Vol. 24, Issue 8
  • DOI: 10.1101/gr.170720.113

Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots
journal, February 2010

  • Moore, M. J.; Soltis, P. S.; Bell, C. D.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 10
  • DOI: 10.1073/pnas.0907801107

Analysis of the function of two circadian-regulated CONSTANS-LIKE genes: Analysis of Arabidopsis CONSTANS-LIKE genes
journal, April 2001


Convergent transcriptional specializations in the brains of humans and song-learning birds
journal, December 2014


Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification
journal, September 1996


Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research
journal, April 2016


The genome sequence of the orchid Phalaenopsis equestris
journal, November 2014

  • Cai, Jing; Liu, Xin; Vanneste, Kevin
  • Nature Genetics, Vol. 47, Issue 1
  • DOI: 10.1038/ng.3149

Emerging model systems for functional genomics analysis of Crassulacean acid metabolism
journal, June 2016

  • Hartwell, James; Dever, Louisa V.; Boxall, Susanna F.
  • Current Opinion in Plant Biology, Vol. 31
  • DOI: 10.1016/j.pbi.2016.03.019

Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars
journal, March 2001


Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets
journal, March 2017

  • Zeng, Liping; Zhang, Ning; Zhang, Qiang
  • New Phytologist, Vol. 214, Issue 3
  • DOI: 10.1111/nph.14503

HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014


Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas
journal, January 2017

  • Hu, Yibo; Wu, Qi; Ma, Shuai
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
  • DOI: 10.1073/pnas.1613870114

The Law of Parsimony
journal, January 1919


Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach
journal, April 2013

  • Soltis, D. E.; Mort, M. E.; Latvis, M.
  • American Journal of Botany, Vol. 100, Issue 5
  • DOI: 10.3732/ajb.1300044

The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity
journal, December 2014

  • Magallón, Susana; Gómez‐Acevedo, Sandra; Sánchez‐Reyes, Luna L.
  • New Phytologist, Vol. 207, Issue 2
  • DOI: 10.1111/nph.13264

Evolution along the crassulacean acid metabolism continuum
journal, January 2010

  • Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark
  • Functional Plant Biology, Vol. 37, Issue 11
  • DOI: 10.1071/FP10084

Development and use of bioenergy feedstocks for semi-arid and arid lands
journal, April 2015

  • Cushman, John C.; Davis, Sarah C.; Yang, Xiaohan
  • Journal of Experimental Botany, Vol. 66, Issue 14
  • DOI: 10.1093/jxb/erv087

Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate
journal, September 2013

  • Martins, Marina Camara Mattos; Hejazi, Mahdi; Fettke, Joerg
  • Plant Physiology, Vol. 163, Issue 3
  • DOI: 10.1104/pp.113.226787

Predictable convergence in hemoglobin function has unpredictable molecular underpinnings
journal, October 2016

  • Natarajan, Chandrasekhar; Hoffmann, Federico G.; Weber, Roy E.
  • Science, Vol. 354, Issue 6310
  • DOI: 10.1126/science.aaf9070

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

  • Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana
  • Plant Physiology, Vol. 167, Issue 1
  • DOI: 10.1104/pp.114.251827

Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response
journal, May 2004


PosiGene: automated and easy-to-use pipeline for genome-wide detection of positively selected genes
journal, March 2017

  • Sahm, Arne; Bens, Martin; Platzer, Matthias
  • Nucleic Acids Research, Vol. 45, Issue 11
  • DOI: 10.1093/nar/gkx179

Resolving the Activation Site of Positive Regulators in Plant Phosphoenolpyruvate Carboxylase
journal, February 2014

  • Schlieper, Daniel; Förster, Kerstin; Paulus, Judith K.
  • Molecular Plant, Vol. 7, Issue 2
  • DOI: 10.1093/mp/sst130

An efficient algorithm for large-scale detection of protein families
journal, April 2002


The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis
journal, January 2007

  • Mockler, T. C.; Michael, T. P.; Priest, H. D.
  • Cold Spring Harbor Symposia on Quantitative Biology, Vol. 72, Issue 1
  • DOI: 10.1101/sqb.2007.72.006

Coupled chaperone action in folding and assembly of hexadecameric Rubisco
journal, January 2010

  • Liu, Cuimin; Young, Anna L.; Starling-Windhof, Amanda
  • Nature, Vol. 463, Issue 7278
  • DOI: 10.1038/nature08651

Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression
journal, November 1999


    Works referencing / citing this record:

    Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
    journal, August 2018


    RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum
    journal, November 2018


    CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants
    journal, September 2019

    • Liu, Degao; Chen, Mei; Mendoza, Brian
    • Journal of Experimental Botany, Vol. 70, Issue 22
    • DOI: 10.1093/jxb/erz415

    Contingency and determinism in evolution: Replaying life’s tape
    journal, November 2018

    • Blount, Zachary D.; Lenski, Richard E.; Losos, Jonathan B.
    • Science, Vol. 362, Issue 6415
    • DOI: 10.1126/science.aam5979

    RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum
    journal, November 2018


    Ecophysiology of constitutive and facultative CAM photosynthesis
    journal, February 2019


    CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants
    journal, September 2019

    • Liu, Degao; Chen, Mei; Mendoza, Brian
    • Journal of Experimental Botany, Vol. 70, Issue 22
    • DOI: 10.1093/jxb/erz415

    Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
    journal, August 2018


    Genome-wide phylogenetic and structural analysis reveals the molecular evolution of the ABA receptor gene family
    journal, November 2019

    • Yang, Jing-Fang; Chen, Mo-Xian; Zhang, Jian-Hua
    • Journal of Experimental Botany, Vol. 71, Issue 4
    • DOI: 10.1093/jxb/erz511