Organ-enriched gene expression during floral morphogenesis in wild barley.

Floral morphology varies considerably between dicots and monocots. The ABCDE model explaining how floral organ development is controlled was formulated using core eudicots and applied to grass crops. Barley (Hordeum. vulgare) has unique floral morphogenesis. Wild barley (H. vulgare ssp. spontaneum), which is the immediate ancestor of cultivated barley (H. vulgare ssp. vulgare), contains a rich reservoir of genetic diversity. However, the wild barley genes involved in floral organ development are still relatively uncharacterized. In this study, we generated an organ-specific transcriptome atlas for wild barley floral organs. Genome-wide transcription profiles indicated that 22 838 protein-coding genes were expressed in at least one organ. These genes were grouped into seven clusters according to the similarities in their expression patterns. Moreover, 5619 genes exhibited organ-enriched expression, 677 of which were members of 47 transcription factor families. Gene ontology analyses suggested that the functions of the genes with organ-enriched expression influence the biological processes in floral organs. The co-expression regulatory network showed that the expression of 690 genes targeted by MADS-box proteins was highly positively correlated with the expression of ABCDE model genes during floral morphogenesis. Furthermore, the expression of 138 genes was specific to the wild barley OUH602 genome and not the Morex genome; most of these genes were highly expressed in the glume, awn, lemma, and palea. This study revealed the global gene expression patterns underlying floral morphogenesis in wild barley. On the basis of the study findings, a molecular mechanism controlling floral morphology in barley was proposed.

[1]  T. Komatsuda,et al.  Genome-Wide Analysis of Snf2 Gene Family Reveals Potential Role in Regulation of Spike Development in Barley , 2022, International journal of molecular sciences.

[2]  Nan Wang,et al.  OsFLA1 encodes a fasciclin-like arabinogalactan protein and affects pollen exine development in rice , 2022, TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik.

[3]  Liu Yang,et al.  Rice SEPALLATA Genes OsMADS5 and OsMADS34 Cooperate to Limit Inflorescence Branching by Repressing the TERMINAL FLOWER1-like Gene RCN4. , 2021, The New phytologist.

[4]  Dabing Zhang,et al.  SMALL REPRODUCTIVE ORGANS, a SUPERMAN-like transcription factor, regulates stamen and pistil growth in rice. , 2021, New Phytologist.

[5]  Honghong Hu,et al.  Expression Pattern and Functional Analyses of Arabidopsis Guard Cell-Enriched GDSL Lipases , 2021, Frontiers in Plant Science.

[6]  R. Burton,et al.  Transcript Profiling of MIKCc MADS-Box Genes Reveals Conserved and Novel Roles in Barley Inflorescence Development , 2021, Frontiers in Plant Science.

[7]  G. Haberer,et al.  Chromosome-scale assembly of wild barley accession “OUH602” , 2021, G3.

[8]  Matthew R. Tucker,et al.  MADS1 maintains barley spike morphology at high ambient temperatures , 2021, Nature Plants.

[9]  J. Grimwood,et al.  Long-read sequence assembly: a technical evaluation in barley , 2021, The Plant cell.

[10]  P. Langridge,et al.  The barley pan-genome reveals the hidden legacy of mutation breeding , 2020, Nature.

[11]  Kazuhiro Sato History and future perspectives of barley genomics , 2020, DNA research : an international journal for rapid publication of reports on genes and genomes.

[12]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[13]  Shiyou Lü,et al.  GDSL lipase Occluded Stomatal Pore 1 is required for wax biosynthesis and stomatal cuticular ledge formation. , 2020, The New phytologist.

[14]  Lixin Zhang,et al.  The spike plays important roles in the drought tolerance as compared to the flag leaf through the phenylpropanoid pathway in wheat. , 2020, Plant physiology and biochemistry : PPB.

[15]  Jun Xiao,et al.  LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate , 2020, Nature Communications.

[16]  T. Schnurbusch,et al.  Developmental pathways for shaping spike inflorescence architecture in barley and wheat. , 2019, Journal of integrative plant biology.

[17]  J. Stiller,et al.  A pan-transcriptome analysis shows that disease resistance genes have undergone more selection pressure during barley domestication , 2019, BMC Genomics.

[18]  J. Dubcovsky,et al.  Wheat VRN1, FUL2 and FUL3 play critical and redundant roles in spikelet development and spike determinacy , 2019, Development.

[19]  K. Kaufmann,et al.  Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana , 2018, Nature Communications.

[20]  G. An,et al.  OsMADS6 Controls Flower Development by Activating Rice FACTOR OF DNA METHYLATION LIKE11[OPEN] , 2018, Plant Physiology.

[21]  Matthew R. Tucker,et al.  Dissecting the role of MADS-box genes in monocot floral development and diversity , 2018, Journal of experimental botany.

[22]  D. Latrasse,et al.  At-MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM ACTIVITY, a Conserved Missing Link in the Regulation of Floral Meristem Termination in Arabidopsis and Tomato , 2018, Plant Cell.

[23]  T. Komatsuda,et al.  A GDSL‐motif esterase/acyltransferase/lipase is responsible for leaf water retention in barley , 2017, Plant direct.

[24]  B. Glover,et al.  The Evolution of Diverse Floral Morphologies , 2017, Current Biology.

[25]  D. Smyth Wrinkles on Sepals: Cuticular Ridges Form when Cuticle Production Outpaces Epidermal Cell Expansion. , 2017, Molecular plant.

[26]  Chengcai Chu,et al.  Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase , 2017, Nature Plants.

[27]  F. Parcy,et al.  A flower is born: an update on Arabidopsis floral meristem formation. , 2017, Current opinion in plant biology.

[28]  Xiaochen Wang,et al.  A β-Ketoacyl-CoA Synthase Is Involved in Rice Leaf Cuticular Wax Synthesis and Requires a CER2-LIKE Protein as a Cofactor1 , 2016, Plant Physiology.

[29]  F. Madueño,et al.  Altered expression of the bZIP transcription factor DRINK ME affects growth and reproductive development in Arabidopsis thaliana. , 2016, The Plant journal : for cell and molecular biology.

[30]  Ge Gao,et al.  PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants , 2016, Nucleic Acids Res..

[31]  Roland Eils,et al.  Complex heatmaps reveal patterns and correlations in multidimensional genomic data , 2016, Bioinform..

[32]  G. Theißen,et al.  MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution , 2016, Development.

[33]  T. Komatsuda,et al.  Alanine aminotransferase controls seed dormancy in barley , 2016, Nature Communications.

[34]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[35]  T. Komatsuda,et al.  Mitogen-Activated Protein Kinase Kinase 3 Regulates Seed Dormancy in Barley , 2016, Current Biology.

[36]  K. Kaufmann,et al.  Molecular mechanisms of floral organ specification by MADS domain proteins. , 2016, Current opinion in plant biology.

[37]  T. Komatsuda,et al.  Evolution of the Grain Dispersal System in Barley , 2015, Cell.

[38]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[39]  H. Yoshida,et al.  Interpreting lemma and palea homologies: a point of view from rice floral mutants , 2015, Front. Plant Sci..

[40]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[41]  Pedro Madrigal,et al.  Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development , 2014, Genome Biology.

[42]  B. Glover,et al.  Understanding Flowers and Flowering, Second Edition , 2014 .

[43]  Chentao Lin,et al.  Multiple bHLH Proteins form Heterodimers to Mediate CRY2-Dependent Regulation of Flowering-Time in Arabidopsis , 2013, PLoS genetics.

[44]  K. Murai Homeotic Genes and the ABCDE Model for Floral Organ Formation in Wheat , 2013, Plants.

[45]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[46]  H. Kanamori,et al.  A SHORT INTERNODES (SHI) family transcription factor gene regulates awn elongation and pistil morphology in barley , 2012, Journal of experimental botany.

[47]  H. Yoshida,et al.  Inflorescence Meristem Identity in Rice Is Specified by Overlapping Functions of Three AP1/FUL-Like MADS Box Genes and PAP2, a SEPALLATA MADS Box Gene[C][W] , 2012, Plant Cell.

[48]  H. Yoshida Is the lodicule a petal: molecular evidence? , 2012, Plant science : an international journal of experimental plant biology.

[49]  Thomas L. Slewinski,et al.  SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors , 2012, Proceedings of the National Academy of Sciences.

[50]  Shujing Liu,et al.  Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development , 2012, Proceedings of the National Academy of Sciences.

[51]  Fionn Murtagh,et al.  Ward’s Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward’s Criterion? , 2011, Journal of Classification.

[52]  H. Yoshida,et al.  Flower development in rice. , 2011, Journal of experimental botany.

[53]  A. Paolacci,et al.  Molecular aspects of flower development in grasses , 2011, Sexual Plant Reproduction.

[54]  Hanbo Chen,et al.  VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R , 2011, BMC Bioinformatics.

[55]  G. Müller,et al.  Role of photosynthesis and analysis of key enzymes involved in primary metabolism throughout the lifespan of the tobacco flower. , 2010, Journal of experimental botany.

[56]  Roger P. Wise,et al.  Drought response in the spikes of barley: gene expression in the lemma, palea, awn, and seed , 2010, Functional & Integrative Genomics.

[57]  H. Kong,et al.  The SEPALLATA-Like Gene OsMADS34 Is Required for Rice Inflorescence and Spikelet Development1[C][W][OA] , 2010, Plant Physiology.

[58]  Z. Schwarz‐Sommer,et al.  Floral organ identity: 20 years of ABCs. , 2010, Seminars in cell & developmental biology.

[59]  T. Komatsuda,et al.  Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage , 2009, Proceedings of the National Academy of Sciences.

[60]  Davis J. McCarthy,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[61]  T. Abebe,et al.  Comparative Transcriptional Profiling Established the Awn as the Major Photosynthetic Organ of the Barley Spike While the Lemma and the Palea Primarily Protect the Seed , 2009 .

[62]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[63]  K. Takeda,et al.  An application of high-throughput SNP genotyping for barley genome mapping and characterization of recombinant chromosome substitution lines , 2009, Theoretical and Applied Genetics.

[64]  H. Yoshida,et al.  Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. , 2008, Plant & cell physiology.

[65]  T. Komatsuda,et al.  The Importance of Barley Genetics and Domestication in a Global Perspective , 2007, Annals of botany.

[66]  Lokesh Kumar,et al.  Mfuzz: A software package for soft clustering of microarray data , 2007, Bioinformation.

[67]  R. Elbaum,et al.  The Role of Wheat Awns in the Seed Dispersal Unit , 2007, Science.

[68]  Andreas Graner,et al.  Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene , 2007, Proceedings of the National Academy of Sciences.

[69]  C. Dumas,et al.  BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size , 2006, The EMBO journal.

[70]  G. An,et al.  Functional Diversification of the Two C-Class MADS Box Genes OSMADS3 and OSMADS58 in Oryza sativa[W][OA] , 2005, The Plant Cell Online.

[71]  Kevin P. Smith,et al.  Quantitative Trait Loci for Multiple Disease Resistance in Wild Barley , 2005 .

[72]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[73]  Ning Sun,et al.  Organ-Specific Expression of Arabidopsis Genome during Development1[w] , 2005, Plant Physiology.

[74]  Detlef Weigel,et al.  The Floral Regulator LEAFY Evolves by Substitutions in the DNA Binding Domain , 2005, Science.

[75]  P. Robles,et al.  The SEP4 Gene of Arabidopsis thaliana Functions in Floral Organ and Meristem Identity , 2004, Current Biology.

[76]  E. Meyerowitz,et al.  The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS , 2004, Nature.

[77]  K. Okada,et al.  RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana , 2003, Development.

[78]  A. Bacic,et al.  The Fasciclin-Like Arabinogalactan Proteins of Arabidopsis. A Multigene Family of Putative Cell Adhesion Molecules1 , 2003, Plant Physiology.

[79]  P. Shannon,et al.  Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks , 2003 .

[80]  Jian-Kang Zhu,et al.  The Arabidopsis SOS5 Locus Encodes a Putative Cell Surface Adhesion Protein and Is Required for Normal Cell Expansion Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007872. , 2003, The Plant Cell Online.

[81]  Heinz Saedler,et al.  Plant biology: Floral quartets , 2001, Nature.

[82]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[83]  G. Ditta,et al.  B and C floral organ identity functions require SEPALLATA MADS-box genes , 2000, Nature.

[84]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[85]  L. Jermiin,et al.  Genome-wide analysis of MIKC-type MADS-box genes in wheat: pervasive duplications, functional conservation and putative neofunctionalization. , 2019, The New phytologist.

[86]  G. Theißen,et al.  The ABCs of flower development: mutational analysis of AP1/FUL‐like genes in rice provides evidence for a homeotic (A)‐function in grasses , 2017, The Plant journal : for cell and molecular biology.

[87]  Trupti M. Kodinariya,et al.  Review on determining number of Cluster in K-Means Clustering , 2013 .

[88]  Ira M. Hall,et al.  BEDTools: a flexible suite of utilities for comparing genomic features , 2010, Bioinform..

[89]  U. Lundqvist,et al.  New and revised descriptions of barley genes , 1997 .