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      The R2R3-MYB gene family in banana (Musa acuminata): Genome-wide identification, classification and expression patterns

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          Abstract

          The R2R3-MYB genes comprise one of the largest transcription factor gene families in plants, playing regulatory roles in plant-specific developmental processes, defense responses and metabolite accumulation. To date MYB family genes have not yet been comprehensively identified in the major staple fruit crop banana. In this study, we present a comprehensive, genome-wide analysis of the MYB genes from Musa acuminata DH-Pahang (A genome). A total of 285 R2R3-MYB genes as well as genes encoding three other classes of MYB proteins containing multiple MYB repeats were identified and characterised with respect to structure and chromosomal organisation. Organ- and development-specific expression patterns were determined from RNA-Seq data. For 280 M. acuminata MYB genes for which expression was found in at least one of the analysed samples, a variety of expression patterns were detected. The M. acuminata R2R3-MYB genes were functionally categorised, leading to the identification of seven clades containing only M. acuminata R2R3-MYBs. The encoded proteins may have specialised functions that were acquired or expanded in Musa during genome evolution. This functional classification and expression analysis of the MYB gene family in banana establishes a solid foundation for future comprehensive functional analysis of MaMYBs and can be utilized in banana improvement programmes.

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          The R2R3-MYB gene family in Arabidopsis thaliana.

          MYB factors represent a family of proteins that include the conserved MYB DNA-binding domain. In contrast to animals, plants contain a MYB-protein subfamily that is characterised by the R2R3-type MYB domain. 'Classical' MYB factors, which are related to c-Myb, seem to be involved in the control of the cell cycle in animals, plants and other higher eukaryotes. Systematic screens for knockout mutations in MYB genes, followed by phenotypic analyses and the dissection of mutants with interesting phenotypes, have started to unravel the functions of the 125 R2R3-MYB genes in Arabidopsis thaliana. R2R3-type MYB genes control many aspects of plant secondary metabolism, as well as the identity and fate of plant cells.
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            The banana (Musa acuminata) genome and the evolution of monocotyledonous plants.

            Bananas (Musa spp.), including dessert and cooking types, are giant perennial monocotyledonous herbs of the order Zingiberales, a sister group to the well-studied Poales, which include cereals. Bananas are vital for food security in many tropical and subtropical countries and the most popular fruit in industrialized countries. The Musa domestication process started some 7,000 years ago in Southeast Asia. It involved hybridizations between diverse species and subspecies, fostered by human migrations, and selection of diploid and triploid seedless, parthenocarpic hybrids thereafter widely dispersed by vegetative propagation. Half of the current production relies on somaclones derived from a single triploid genotype (Cavendish). Pests and diseases have gradually become adapted, representing an imminent danger for global banana production. Here we describe the draft sequence of the 523-megabase genome of a Musa acuminata doubled-haploid genotype, providing a crucial stepping-stone for genetic improvement of banana. We detected three rounds of whole-genome duplications in the Musa lineage, independently of those previously described in the Poales lineage and the one we detected in the Arecales lineage. This first monocotyledon high-continuity whole-genome sequence reported outside Poales represents an essential bridge for comparative genome analysis in plants. As such, it clarifies commelinid-monocotyledon phylogenetic relationships, reveals Poaceae-specific features and has led to the discovery of conserved non-coding sequences predating monocotyledon-eudicotyledon divergence.
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              Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins.

              In-depth analysis of protein-protein interaction specificities of the MYB protein family of Arabidopsis thaliana revealed a conserved amino acid signature ([DE]Lx(2)[RK]x(3)Lx(6)Lx(3)R) as the structural basis for interaction between MYB and R/B-like BHLH proteins. The motif has successfully been used to predict new MYB/BHLH interactions for A. thaliana proteins, it allows to discriminate between even closely related MYB proteins and it is conserved amongst higher plants. In A. thaliana, the motif is shared by fourteen R2R3 MYB proteins and six 1R MYB proteins. It is located on helices 1 and 2 of the R3 repeat and forms a characteristic surface-exposed pattern of hydrophobic and charged residues. Single-site mutation of any amino acid of the signature impairs the interaction. Two particular amino acids have been determined to account for most of the interaction stability. Functional specificity of MYB/BHLH complexes was investigated in vivo by a transient DFR promoter activation assay. Residues stabilizing the MYB/BHLH interaction were shown to be critical for promoter activation. By virtue of proved and predicted interaction specificities, this study provides a comprehensive survey of the MYB proteins that interact with R/B-like BHLH proteins potentially involved in the TTG1-dependent regulatory interaction network. The results are discussed with respect to multi-functionality, specificity and redundancy of MYB and BHLH protein function.
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                Author and article information

                Contributors
                Role: Data curationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – original draft
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                6 October 2020
                2020
                : 15
                : 10
                : e0239275
                Affiliations
                [1 ] Faculty of Biology, Genetics and Genomics of Plants, Bielefeld University, Bielefeld, Germany
                [2 ] National Institute of Plant Genome Research, New Delhi, India
                Aberystwyth University, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-3321-7471
                http://orcid.org/0000-0002-7635-3473
                http://orcid.org/0000-0002-9261-2279
                Article
                PONE-D-20-03155
                10.1371/journal.pone.0239275
                7537896
                33021974
                4cecf230-1ac8-4e59-a488-5eb5ebad7eda
                © 2020 Pucker et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 February 2020
                : 3 September 2020
                Page count
                Figures: 2, Tables: 2, Pages: 27
                Funding
                The research stay of AP at Weisshaar lab was supported by a grant from Alexander von Humbold Foundation (AvH) (AvH-IND/1184925). The publication costs were supported by Deutsche Forschungsgemeinschaft (DFG) and the Open Access Publication Fund of Bielefeld University. This is a general fund of Bielefeld University with DFG support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cellular Stress Responses
                Physical Sciences
                Chemistry
                Chemical Compounds
                Lignin
                Biology and Life Sciences
                Physiology
                Plant Physiology
                Meristems
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Meristems
                Biology and life sciences
                Biochemistry
                Proteins
                DNA-binding proteins
                Transcription Factors
                Biology and Life Sciences
                Genetics
                Gene Expression
                Gene Regulation
                Transcription Factors
                Biology and Life Sciences
                Biochemistry
                Proteins
                Regulatory Proteins
                Transcription Factors
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Bananas
                Biology and Life Sciences
                Biochemistry
                Lipids
                Oils
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Walls
                Biology and Life Sciences
                Genetics
                Gene Expression
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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