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Comprehensive analysis of 1R- and 2R-MYBs reveals novel genic and protein features, complex organisation, selective expansion and insights into evolutionary tendencies

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Abstract

Myeloblastosis (MYB) family, the largest plant transcription factor family, has been subcategorised based on the number and type of repeats in the MYB domain. In spite of several reports, evolution of MYB genes and repeats remains enigmatic. Brassicaceae members are endowed with complex genomes, including dysploidy because of its unique history with multiple rounds of polyploidisation, genomic fractionations and rearrangements. The present study is an attempt to gain insights into the complexities of MYB family diversity, understand impacts of genome evolution on gene families and develop an evolutionary framework to understand the origin of various subcategories of MYB gene family. We identified and analysed 1129 MYBs that included 1R-, 2R-, 3R- and atypical-MYBs across sixteen species representing protists, fungi, animals and plants and exclude MYB identified from Brassicaceae except Arabidopsis thaliana; in addition, a total of 1137 2R-MYB genes from six Brassicaceae species were also analysed. Comparative analysis revealed predominance of 1R-MYBs in protists, fungi, animals and lower plants. Phylogenetic reconstruction and analysis of selection pressure suggested ancestral nature of R1-type repeat containing 1R-MYBs that might have undergone intragenic duplication to form multi-repeat MYBs. Distinct differences in gene structure between 1R-MYB and 2R-MYBs were observed regarding intron number, the ratio of gene length to coding DNA sequence (CDS) length and the length of exons encoding the MYB domain. Conserved as well as novel and lineage-specific intron phases were identified. Analyses of physicochemical properties revealed drastic differences indicating functional diversification in MYBs. Phylogenetic reconstruction of 1R- and 2R-MYB genes revealed a shared structure–function relationship in clades which was supported when transcriptome data was analysed in silico. Comparative genomics to study distribution pattern and mapping of 2R-MYBs revealed congruency and greater degree of synteny and collinearity among closely related species. Micro-synteny analysis of genomic segments revealed high conservation of genes that are immediately flanking the surrounding tandemly organised 2R-MYBs along with instances of local duplication, reorganisations and genome fractionation. In summary, polyploidy, dysploidy, reshuffling and genome fractionation were found to cause loss or gain of 2R-MYB genes. The findings need to be supported with functional validation to understand gene structure–function relationship along the evolutionary lineage and adaptive strategies based on comparative functional genomics in plants.

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Funding

The award”” of JRF/SRF from UGC to Mukund Lal, from CSIR to Nishu Chahar, and Shobha Yadav, and SRF from DBT (BT/PR18086/BPA/118/186/2016) to Ekta Bhardwaj is gratefully acknowledged. Sandip Das is financially supported by the Institute of Eminence (IoE), University of Delhi (IoE/FRP/LS/2020/27).

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Authors and Affiliations

  1. Department of Botany, University of Delhi, Delhi, 110007, India

    Mukund Lal, Ekta Bhardwaj, Nishu Chahar, Shobha Yadav & Sandip Das

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  1. Mukund Lal
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  2. Ekta Bhardwaj
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  3. Nishu Chahar
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Contributions

ML and SD designed the study. ML performed all analysis with help from EB and NC (identification of homologs, analysis of genic structure and features, phylogeny and protein attributes) and SY (identification of tandem genes and synteny). ML and SD analysed all data and wrote the MS. All authors have read and agree with the findings.

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Correspondence to Sandip Das.

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Supplementary Information

Below is the link to the electronic supplementary material.

10142_2022_836_MOESM1_ESM.pdf

Supplementary file1 (PDF 1328 kb) Phylogram of 2R-MYBs to identify orthologs and paralogs from A. thaliana-A. lyrata [A]; A. thaliana-C. rubella [B]; A. thaliana-C. sativa [C]; A. thaliana-E. salsugineum [D]; and A. thaliana-B. rapa [E].

10142_2022_836_MOESM2_ESM.pdf

Supplementary file2 (PDF 4914 kb) Mapping of distribution and organisation of 1R-MYBs on pseudochromosomes of M. polymorpha, S. moellendorffii, P. abies, A. trichopoda, P. patens, Z. mays, and A. thaliana [A-G]; and 2R-MYB genes on pseudochromosomes of A. thaliana, A. lyrata, C. rubella, C. sativa, and E. salsugineum [H-L].

10142_2022_836_MOESM3_ESM.pdf

Supplementary file3 (PDF 512 kb) Physico-chemical properties of 1R-MYBs in eight plant species and 2R-MYBs in six Brassicaceae species. Bar graphs represent molecular weight of 1R-MYB [A] genes are greater than 2R-MYBs [D]; pI values range from 4 to 10 in both 1R- and 2R-MYBs [B and E]; and GRAVY values for most 1R-MYB and 2R-MYB genes range from -1.25 to -0.25 and -1.0 to -0.5, respectively [C and F].

10142_2022_836_MOESM4_ESM.pdf

Supplementary file4 (PDF 428 kb) Length and position of MYB domain in 1R-MYBs from eight plant species and 2R-MYBs from six Brassicaceae species. Bar graphs show that the length of most 1R-MYB and 2R-MYB genes range from 40 aa to 60 aa and 95 aa to 100 aa, respectively [A and C]; besides the position of the MYB domain in the most 1R- and 2R-MYBs is towards N-terminal region, whereas several 1R-MYB genes have MYB-domain positioned at the centre or towards the C-terminal [B and D].

10142_2022_836_MOESM5_ESM.pdf

Supplementary file5 (PDF 1091 kb) Exons-intron structure, intron phases, and conserved MYB domain using genomic sequences, CDS, and coordinates of MYB domain repeat sequences of 1R-MYBs from eight plant species i.e., C. reinhardtii [A], M. polymorpha [B], P. patens [C], S. moellendorffii [D], P. abies [E], A. trichopoda [F], Z. mays [G], and A. thaliana [H]; and 2R-MYBs from 6 Brassicaceae species i.e., A. thaliana [I], A. lyrata [J], C. rubella [K], C. sativa [L], E. salsugineum [M], and B. rapa [N].

10142_2022_836_MOESM6_ESM.pdf

Supplementary file6 (PDF 349 kb) Phylogenetic reconstruction of MYB repeat sequences (R1, R2 and R3-type) using Neighbor-Joining method with JTT matrix-based model

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Supplementary file7 (PDF 203 kb) Clade wise representation of the conserved MYB domain and C-terminal motifs of 2R-MYBs from A. thaliana

10142_2022_836_MOESM8_ESM.pdf

Supplementary file8 (PDF 1092 kb) Phylogenetic reconstruction of 2R-MYB genes from A. thaliana using Neighbor-Joining method with JTT matrix-based model displays extensive paralogy; clustering based on sequence similarity and similar gene features; and homologs in a given cluster also share functional similarity.

10142_2022_836_MOESM9_ESM.pdf

Supplementary file9 (PDF 2128 kb) Clade-wise alignment of the MYB domain with R2 and R3 repeats and web-logo showing conserved and regularly spaced Tryptophan residues (W) in A. thaliana 2R-MYB genes.

10142_2022_836_MOESM10_ESM.pdf

Supplementary file10 (PDF 957 kb) Heat-maps showing differential expression of thirteen 2R-MYB genes from A. thaliana under three abiotic stress conditions-cold [A], salt [B], and drought [C]. Blue and yellow colour represent the least and the highest Z-score, respectively. The downregulation and upregulation of the gene expression are represented as red and green arrows, respectively.

10142_2022_836_MOESM11_ESM.pdf

Supplementary file11 (PDF 510 kb) Comparative genomics of tandemly organised 2R-MYBs -AtMYB23-AtMYB24-AtMYB115, and AtMYB104-AtMYB81 [A], employing micro-synteny analysis using ca. 100 kb genomic segments across different genomes of Brassicaceae reveals gene losses, duplication and rearrangements [B-C]. Genes unique to a particular genomic segment is marked by black arrows. Larger and coloured arrows represent tandem 2R-MYB genes under investigation. Smaller coloured arrows represent genes that are conserved across at least two genomic segments. Blue rectangle represents duplicated genes whereas red circle represents the most abundant gene.

Supplementary file12 (PDF 15 kb) Tabulation of loss of 2R-MYB genes in Brassicaceae

10142_2022_836_MOESM13_ESM.pdf

Supplementary file13 (PDF 1599 kb) Distribution of 2R-MYBs across the 24-genomic blocks (A-X) across Brassicaceae. Homologous blocks are boxed with similar colours.

10142_2022_836_MOESM14_ESM.xlsx

Supplementary file14 (XLSX 277 kb) Identification of all MYB genes (1R-, 2R-, 3R- and atypical-MYBs) and their genomic features -number of genes; length of gene, CDS and protein; gene/CDS ratio; intron number and phases; molecular weight; pI values; GRAVY values; MYB domain length and its position across 16 taxa representing protists, fungi, animals and plants.

10142_2022_836_MOESM15_ESM.xlsx

Supplementary file15 (XLSX 618 kb) Identification of 2R-MYB genes and their genomic features such as number of genes; length of gene, CDS and protein; gene/CDS ratio; intron number and phases; molecular weight; pI values; GRAVY values; MYB domain length and its position across 6 taxa representing family Brassicaceae.

10142_2022_836_MOESM16_ESM.docx

Supplementary file16 (DOCX 19 kb) Summary of 3D-structure models of clade-wise consensus MYB domain sequences of 1R-MYBs [A] and 2R-MYBs [B] from A. thaliana.

10142_2022_836_MOESM17_ESM.xlsx

Supplementary file17 (XLSX 37 kb) Compiled information about the paralogy, track-files, and label-files of 1R-MYBs and 2R-MYBs from A. thaliana.

10142_2022_836_MOESM18_ESM.xlsx

Supplementary file18 (XLSX 1098 kb) Analysis of the frequency distributions of synonymous substitutions (Ks) and its ratio with non-synonymous substitutions (Ka/Ks; ω) for 1R-MYB paralogs in A. thaliana; 2R-MYB paralogs in A. thaliana and their orthologs in A. lyrata, C. rubella, C. sativa, E. salsugineum, and B. rapa

10142_2022_836_MOESM19_ESM.xlsx

Supplementary file19 (XLSX 34 kb) Normalised microarray expression data for 13 selected A. thaliana 2R-MYB genes belonging to clade 2 (AtMYB49, AtMYB74 and AtMYB102), clade 6 (AtMYB10, AtMYB13, AtMYB14, AtMYB15, AtMYB60 and AtMYB72) and clade 14 (AtMYB44, AtMYB70, AtMYB73 and AtMYB77) that act as regulators under cold, salt and drought stress conditions.

10142_2022_836_MOESM20_ESM.xlsx

Supplementary file20 (XLSX 58 kb) Gene list for Micro-synteny analysis of the 2R-MYB gene pair AtMYB113-AtMYB114-AtMYB90.

Supplementary file21 (XLSX 49 kb) Gene list for micro-synteny analysis of the 2R-MYB gene pair AtMYB104-AtMYB81.

Supplementary file22 (XLSX 51 kb) Gene list for micro-synteny analysis of the 2R-MYB gene pair AtMYB29-AtMYB76.

10142_2022_836_MOESM23_ESM.xlsx

Supplementary file23 (XLSX 40 kb) Gene list for micro-synteny analysis of the 2R-MYB gene pair AtMYB23-AtMYB24-AtMYB115.

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Lal, M., Bhardwaj, E., Chahar, N. et al. Comprehensive analysis of 1R- and 2R-MYBs reveals novel genic and protein features, complex organisation, selective expansion and insights into evolutionary tendencies. Funct Integr Genomics 22, 371–405 (2022). https://doi.org/10.1007/s10142-022-00836-w

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