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MIKCC-type MADS-box genes in Rosa chinensis: the remarkable expansion of ABCDE model genes and their roles in floral organogenesis.

ABSTRACT: MIKCC-type MADS-box (MIKCC) genes encode transcription factors that have crucial roles in controlling floral organogenesis and flowering time in plants. Although this gene family has been well characterized in many plant species, its evolutionary and comprehensive functional analysis in rose is lacking. In this study, 58 non-redundant MIKCC uni-transcripts were extensively identified from rose transcriptomes. Phylogenetic analysis placed these genes into 12 clades with their Arabidopsis and strawberry counterparts, and revealed that ABCDE model (including AP1/FUL, AP3/PI, AG, and SEP clades), and SOC1 and AGL6 clade genes have remarkably expanded in Rosa chinensis, whereas genes from the FLC and AGL17 clades were undetectable. Sequence alignments suggest that the AP3/PI clade may contribute to more specific functions in rose due to a high variation of amino acid residues within its MADS-box domains. A comparative analysis of gene expression in specific floral organ differentiation stages and floral organs between R. chinensis cv. Old Blush and the closely related mutant genotype R. chinensis cv. Viridiflora (floral organs mutated into leaf-like structures) further revealed the roles of ABCDE model genes during floral organogenesis in rose. Analysis of co-expression networks provided an overview of the regulatory mechanisms of rose MIKCC genes and shed light on both the prominent roles of AP3/PI clade genes in floral organogenesis and the roles of RcAGL19, RcAGL24, and RcSOC1 in regulating floral transition in rose. Our analyses provide an overall insight of MIKCC genes in rose and their potential roles in floral organogenesis.

SUBMITTER: Liu J

PROVIDER: S-EPMC5928068 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe morphological diversity of flower organs is closely related to functional divergence within the MADS-box gene family. Bryophytes and seedless vascular plants have MADS-box genes but do not have ABCDE or AGAMOUS-LIKE6 (AGL6) genes. ABCDE and AGL6 genes belong to the subgroup of MADS-box genes. Previous works suggest that the B gene was the first ABCDE and AGL6 genes to emerge in plant but there are no mentions about the probable origin time of ACDE and AGL6 genes. Here, we collected ABCDE and AGL6 gene 381 protein sequences and 361 coding sequences from gymnosperms and angiosperms and reconstructed a complete Bayesian phylogeny of these genes. In this study, we want to clarify the probable origin time of ABCDE and AGL6 genes is a great help for understanding the role of the formation of the flower, which can decipher the forming order of MADS-box genes in the future.ResultsThese genes appeared to have been under purifying selection and their evolutionary rates are not significantly different from each other. Using the Bayesian evolutionary analysis by sampling trees (BEAST) tool, we estimated that: the mutation rate of the ABCDE and AGL6 genes was 2.617 × 10-3 substitutions/site/million years, and that B genes originated 339 million years ago (MYA), CD genes originated 322 MYA, and A genes shared the most recent common ancestor with E/AGL6 296 MYA, respectively.ConclusionsThe phylogeny of ABCDE and AGL6 genes subfamilies differed. The APETALA1 (AP1 or A gene) subfamily clustered into one group. The APETALA3/PISTILLATA (AP3/PI or B genes) subfamily clustered into two groups: the AP3 and PI clades. The AGAMOUS/SHATTERPROOF/SEEDSTICK (AG/SHP/STK or CD genes) subfamily clustered into a single group. The SEPALLATA (SEP or E gene) subfamily in angiosperms clustered into two groups: the SEP1/2/4 and SEP3 clades. The AGL6 subfamily clustered into a single group. Moreover, ABCDE and AGL6 genes appeared in the following order: AP3/PI → AG/SHP/STK → AGL6/SEP/AP1. In this study, we collected candidate sequences from gymnosperms and angiosperms. This study highlights important events in the evolutionary history of the ABCDE and AGL6 gene families and clarifies their evolutionary path.

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MIKCC-type MADS-box genes in Rosa chinensis: the remarkable expansion of ABCDE model genes and their roles in floral organogenesis.

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