The first released available genome of the common ice plant ( Mesembryanthemum crystallinum L.) extended the research region on salt tolerance, C 3-CAM photosynthetic conversion, and halophilism

Background: The common ice plant (Mesembryanthemum crystallinum L.) is an annual herb belonging to the genus Mesembryanthemum of the family Aizoaceae, native to Southern Africa. Methods: We performed shotgun genome paired-end sequencing using the Illumina platform to determine the genome sequence of the ice plants. We assembled the whole genome sequences using the genome assembler “ALGA” and “Redundans”, then released them as available genomic information. Finally, we mainly estimated the potential genomic function by the homology search method. Results: A draft genome was generated with a total length of 286 Mb corresponding to 79.2% of the estimated genome size (361 Mb), consisting of 49,782 contigs. It encompassed 93.49% of the genes of terrestrial higher plants, 99.5% of the ice plant transcriptome, and 100% of known DNA sequences. In addition, 110.9 Mb (38.8%) of repetitive sequences and untranslated regions, 971 tRNA, and 100 miRNA loci were identified, and their effects on stress tolerance and photosynthesis were investigated. Molecular phylogenetic analysis based on ribosomal DNA among 26 kinds of plant species revealed genetic similarity between the ice plant and poplar, which have salt tolerance. Overall, 35,702 protein-coding regions were identified in the genome, of which 56.05% to 82.59% were annotated and submitted to domain searches and gene ontology (GO) analyses, which found that eighteen GO terms stood out among five plant species. These terms were related to biological defense, growth, reproduction, transcription, post-transcription, and intermembrane transportation, regarded as one of the fundamental results of using the utilized ice plant genome. Conclusions: The information that we characterized is useful for elucidation of the mechanism of growth promotion under salinity and reversible conversion of the photosynthetic type from C3 to Crassulacean Acid Metabolism (CAM).

[1]  Ayako Konishi,et al.  NaCl–promoted Respiration and Cell Division in Halophilism of a Halophyte, the Common Ice Plant Mesembryanthemum crystallinum L. , 2022, Journal of the Faculty of Agriculture, Kyushu University.

[2]  Hao Lin,et al.  High‐quality ice plant reference genome analysis provides insights into genome evolution and allows exploration of genes involved in the transition from C3 to CAM pathways , 2022, Plant biotechnology journal.

[3]  Z. Liu,et al.  Full-Length Transcriptome Analysis of the Halophyte Nitraria sibirica Pall , 2022, Genes.

[4]  Y. van de Peer,et al.  Nearby transposable elements impact plant stress gene regulatory networks: a meta-analysis in A. thaliana and S. lycopersicum , 2022, BMC genomics.

[5]  X. Xia,et al.  Advances in 5-Aminolevulinic Acid Priming to Enhance Plant Tolerance to Abiotic Stress , 2022, International journal of molecular sciences.

[6]  A. Gökçe,et al.  The Influence of Salinity Stress on Plants and Their Molecular Mechanisms , 2021, IECPS 2021.

[7]  E. Zdobnov,et al.  BUSCO: Assessing Genomic Data Quality and Beyond , 2021, Current protocols.

[8]  Jianbin Yan,et al.  Isoleucine Enhances Plant Resistance Against Botrytis cinerea via Jasmonate Signaling Pathway , 2021, Frontiers in Plant Science.

[9]  S. Chen,et al.  Nuclear factor Y subunit GmNFYA competes with GmHDA13 for interaction with GmFVE to positively regulate salt tolerance in soybean , 2021, Plant biotechnology journal.

[10]  Aref Alshameri,et al.  Estimation of Genome Size in the Endemic Species Reseda pentagyna and the Locally Rare Species Reseda lutea Using comparative Analyses of Flow Cytometry and K-Mer Approaches , 2021, Plants.

[11]  Sixue Chen,et al.  Proteomics of Homeobox7 Enhanced Salt Tolerance in Mesembryanthemum crystallinum , 2021, International journal of molecular sciences.

[12]  Khalid Rehman Hakeem,et al.  Understanding the Integrated Pathways and Mechanisms of Transporters, Protein Kinases, and Transcription Factors in Plants under Salt Stress , 2021, International journal of genomics.

[13]  Sixue Chen,et al.  Functional Characterization of a Sugar Beet BvbHLH93 Transcription Factor in Salt Stress Tolerance , 2021, International journal of molecular sciences.

[14]  E. Niewiadomska,et al.  Acclimation to salinity in halophytic ice plant prevents a decline of linear electron transport , 2021 .

[15]  H. Drost,et al.  Sensitive protein alignments at tree-of-life scale using DIAMOND , 2021, Nature Methods.

[16]  T. Tang,et al.  Weak Effect of Gypsy Retrotransposon Bursts on Sonneratia alba Salt Stress Gene Expression , 2021, bioRxiv.

[17]  Mervat Shamoon Sadak,et al.  Impact of melatonin and tryptophan on water stress tolerance in white lupine (Lupinus termis L.) , 2021, Physiology and Molecular Biology of Plants.

[18]  Jacek Blazewicz,et al.  Genome-scale de novo assembly using ALGA , 2021, Bioinform..

[19]  Silvio C. E. Tosatto,et al.  Pfam: The protein families database in 2021 , 2020, Nucleic Acids Res..

[20]  T. Tschaplinski,et al.  Biosystems Design to Accelerate C3-to-CAM Progression , 2020, Biodesign research.

[21]  Mario Stanke,et al.  BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database , 2020, bioRxiv.

[22]  Cédric Feschotte,et al.  RepeatModeler2 for automated genomic discovery of transposable element families , 2020, Proceedings of the National Academy of Sciences.

[23]  J. Tőzsér,et al.  Functional Study of the Retrotransposon-Derived Human PEG10 Protease , 2020, International journal of molecular sciences.

[24]  J. Cushman,et al.  Ion accumulation and expression of ion homeostasis-related genes associated with halophilism, NaCl-promoted growth in a halophyte Mesembryanthemum crystallinum L. , 2020, Plant Production Science.

[25]  M. Morokuma,et al.  NaCl-stimulated ATP synthesis in mitochondria of a halophyte Mesembryanthemum crystallinum L. , 2020, Plant Production Science.

[26]  Pei Sun,et al.  A Stress-Associated Protein, PtSAP13, From Populus trichocarpa Provides Tolerance to Salt Stress , 2019, International journal of molecular sciences.

[27]  J. Zhuang,et al.  Genomic and transcriptomic analyses of HD-Zip family transcription factors and their responses to abiotic stress in tea plant (Camellia sinensis). , 2019, Genomics.

[28]  M. Schatz,et al.  GenomeScope 2.0 and Smudgeplots: Reference-free profiling of polyploid genomes , 2019, bioRxiv.

[29]  Li-an Xu,et al.  Roles of the SPL gene family and miR156 in the salt stress responses of tamarisk (Tamarix chinensis) , 2019, BMC Plant Biology.

[30]  Gustavo Isaza,et al.  Retrotransposons in Plant Genomes: Structure, Identification, and Classification through Bioinformatics and Machine Learning , 2019, International journal of molecular sciences.

[31]  F. Ruiz-Espinoza,et al.  Evaluation of Glycosyl-Hydrolases, Phosphatases, Esterases and Proteases as Potential Biomarker for NaCl-Stress Tolerance in Solanum lycopersicum L. Varieties , 2019, Molecules.

[32]  Patricia P. Chan,et al.  tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes , 2019, bioRxiv.

[33]  Olivier Gascuel,et al.  NGPhylogeny.fr: new generation phylogenetic services for non-specialists , 2019, Nucleic Acids Res..

[34]  S. Assmann,et al.  Molecular changes in Mesembryanthemum crystallinum guard cells underlying the C3 to CAM transition , 2019, Plant Molecular Biology.

[35]  Atia B. Amin,et al.  Crassulacean Acid Metabolism Abiotic Stress-Responsive Transcription Factors: a Potential Genetic Engineering Approach for Improving Crop Tolerance to Abiotic Stress , 2019, Front. Plant Sci..

[36]  W. C. Yim,et al.  Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis , 2019, Front. Plant Sci..

[37]  David Ellis,et al.  Current Strategies of Polyploid Plant Genome Sequence Assembly , 2018, Front. Plant Sci..

[38]  W. Yin,et al.  Populus trichocarpa PtNF-YA9, A Multifunctional Transcription Factor, Regulates Seed Germination, Abiotic Stress, Plant Growth and Development in Arabidopsis , 2018, Front. Plant Sci..

[39]  Robert D. Finn,et al.  HMMER web server: 2018 update , 2018, Nucleic Acids Res..

[40]  M. Dassanayake,et al.  Making Epidermal Bladder Cells Bigger: Developmental- and Salinity-Induced Endopolyploidy in a Model Halophyte1[OPEN] , 2018, Plant Physiology.

[41]  Brent S. Pedersen,et al.  Mosdepth: quick coverage calculation for genomes and exomes , 2017, bioRxiv.

[42]  Osamu Nishimura,et al.  gVolante for standardizing completeness assessment of genome and transcriptome assemblies , 2017, Bioinform..

[43]  G. Martin,et al.  iTAK: A Program for Genome-wide Prediction and Classification of Plant Transcription Factors, Transcriptional Regulators, and Protein Kinases. , 2016, Molecular plant.

[44]  Yan Li,et al.  SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation , 2016, PloS one.

[45]  Sixue Chen,et al.  Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses , 2016, Scientific Reports.

[46]  W. C. Yim,et al.  Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings , 2016, Front. Plant Sci..

[47]  Xinguang Zhu,et al.  Evidence for the role of transposons in the recruitment of cis-regulatory motifs during the evolution of C4 photosynthesis , 2016, BMC Genomics.

[48]  H. Bohnert,et al.  Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum. , 2015 .

[49]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[50]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[51]  H. Su,et al.  Overexpression of a Populus trichocarpa H+-pyrophosphatase gene PtVP1.1 confers salt tolerance on transgenic poplar. , 2015, Tree physiology.

[52]  Leszek P. Pryszcz,et al.  Supplementary Figures and Tables , 2012 .

[53]  T. Higashiyama,et al.  RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity , 2015, PloS one.

[54]  R. Kumar,et al.  Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation , 2014, Saudi journal of biological sciences.

[55]  Manzoor Qadir,et al.  Economics of salt-induced land degradation and restoration , 2014 .

[56]  Takuro Tamura,et al.  Plant Genome DataBase Japan (PGDBj): A Portal Website for the Integration of Plant Genome-Related Databases , 2014, Plant & cell physiology.

[57]  Sean R. Eddy,et al.  Infernal 1.1: 100-fold faster RNA homology searches , 2013, Bioinform..

[58]  J. Ohnishi,et al.  Characterization of the Plastidic Phosphate Translocators in the Inducible Crassulacean Acid Metabolism Plant Mesembryanthemum crystallinum , 2013, Bioscience, biotechnology, and biochemistry.

[59]  Yongchao Liu,et al.  Musket: a multistage k-mer spectrum-based error corrector for Illumina sequence data , 2013, Bioinform..

[60]  Valérie Cognat,et al.  PlantRNA, a database for tRNAs of photosynthetic eukaryotes , 2012, Nucleic Acids Res..

[61]  Yutaka Sato,et al.  Role of Transposon-Derived Small RNAs in the Interplay between Genomes and Parasitic DNA in Rice , 2012, PLoS genetics.

[62]  S. Clark,et al.  The RLK/Pelle family of kinases. , 2011, The Plant journal : for cell and molecular biology.

[63]  Carl Kingsford,et al.  A fast, lock-free approach for efficient parallel counting of occurrences of k-mers , 2011, Bioinform..

[64]  György Abrusán,et al.  TEclass - a tool for automated classification of unknown eukaryotic transposable elements , 2009, Bioinform..

[65]  S. Agarie,et al.  Potential of the Common Ice Plant, Mesembryanthemum crystallinum as a New High-Functional Food as Evaluated by Polyol Accumulation , 2009 .

[66]  A. Borland,et al.  Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism1[W][OA] , 2008, Plant Physiology.

[67]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.

[68]  F. Turck,et al.  CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis[W][OA] , 2006, The Plant Cell Online.

[69]  T. Hughes,et al.  Regulation of gene expression by alternative untranslated regions. , 2006, Trends in genetics : TIG.

[70]  S. Agarie.  Possibility of Desalinization of Saline Soils by Common Ice Plant (Mesembryanthemum crystallinum) , 2004 .

[71]  J. Cushman,et al.  Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum. , 2004, Gene.

[72]  Thomas L. Madden,et al.  BLAST: at the core of a powerful and diverse set of sequence analysis tools , 2004, Nucleic Acids Res..

[73]  Ilia J. Leitch,et al.  Comparisons with Caenorhabditis (∼100 Mb) and Drosophila (∼175 Mb) Using Flow Cytometry Show Genome Size in Arabidopsis to be ∼157 Mb and thus ∼25 % Larger than the Arabidopsis Genome Initiative Estimate of ∼125 Mb , 2003 .

[74]  H. G. Nimmo.  The regulation of phosphoenolpyruvate carboxylase in CAM plants. , 2000, Trends in plant science.

[75]  Cushman,et al.  Signaling events leading to crassulacean acid metabolism induction in the common ice plant , 1999, Plant physiology.

[76]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[77]  Howard Griffiths,et al.  Growth and development of Mesembryanthemum crystallinum (Aizoaceae). , 1998, The New phytologist.

[78]  J. Cushman,et al.  Posttranscriptional and Posttranslational Control of Enolase Expression in the Facultative Crassulacean Acid Metabolism Plant Mesembryanthemum crystallinum L , 1995, Plant physiology.

[79]  H. Bohnert,et al.  Direct screening of a small genome : Estimation of the magnitude of plant gene expression changes during adaptation to high salt , 1990, Molecular and General Genetics MGG.

[80]  D. Galbraith,et al.  Developmentally Regulated Systemic Endopolyploid in Succulents with Small Genomes , 1990, Science.

[81]  R. Miller,et al.  Nutrient requirements of suspension cultures of soybean root cells. , 1968, Experimental cell research.

[82]  OUP accepted manuscript , 2022, Nucleic Acids Research.

[83]  M. Berriman,et al.  REAPR: a universal tool for genome assembly evaluation. , 2013, Genome biology.

[84]  Hidetaka Ito.  Small RNAs and regulation of transposons in plants. , 2013, Genes & genetic systems.

[85]  K. Winter,et al.  Seasonal shift from C3 photosynthesis to Crassulacean Acid Metabolism in Mesembryanthemum crystallinum growing in its natural environment , 2004, Oecologia.

[86]  H. Bohnert,et al.  Salt stress in Mesembryanthemum crystallinum L. cell suspensions activates adaptive mechanisms similar to those observed in the whole plant , 1999, Planta.