Origination and selection of ABCDE and AGL6 subfamily MADS-box genes in gymnosperms and angiosperms

Abstract

Background: The 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.

Results: These 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.

Conclusions: The 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.

Keywords: ABCDE gene; AGL6; Evolutionary events; MADS-box gene; Phylogenetic analysis.

Fig. 1

Phylogeny of the ABCDE and AGL6 genes from 27 plant species and 381 classified protein sequences obtained using BEAST. The genes are indicated as follows: AP1, blue; AP3/PI, green; AG/SHP/STK, red; SEP, yellow; AGL6/AGL13, purple; and Type I MADS-box gene as an outgroup, brown. The Bayesian posterior probability values (numbers in black) are shown on the tree. Asterisks (*) represent Poaceae (Oryza sativa: OsMADS14,15,18 and 20; Zea mays: ZmMADS3p, 8, 15, 16, 25, 34 and 50)

Fig. 2

Phylogeny of the ABCDE and AGL6 genes from 27 plant species and 361 classified coding sequences obtained using BEAST. The genes are colored as follows: AP1, blue; AP3/PI, green; AG/SHP/STK, red; SEP, yellow; and AGL6/AGL13, purple. The red values represent the probable origin and divergence time (million years ago, MYA) as calculated using BEAST of the AP1, AP3/PI, AG/SHP/STK, SEP, and AGL6/AGL13 genes in the tree. AP3/PI originated 339 MYA; AG/SHP/STK originated 322 MYA; and AP1, SEP, and AGL6/AGL13 originated 296 MYA. The divergence of SEP and AGL6/13 occurred 269 MYA, and the divergence of AP1 occurred 233 MYA

Fig. 3

Evolution of B-class genes (AP3/PI) and their roles in Arabidopsis thaliana, Oryza sativa, and Ginkgo biloba. Model 1: The progenitor of the B-class gene (B^a) primarily evolved from a PI lineage and generated the AP3 and PI lineages through duplication. However, it evolved the PI in gymnosperm before duplication of the B-class gene generated the AP3 lineage in the angiosperm. Arabidopsis represents Arabidopsis thaliana. Arabidopsis thaliana and Oryza sativa have AP3 and PI. Other angiosperms with the B-class gene also possess AP3 and PI. Model 2: A duplication generated the ancestral (B^a) AP3 and PI lineages and a subsequent duplication; however, the AP3 lineage was subsequently lost in gymnosperms. Arabidopsis represents Arabidopsis thaliana. Arabidopsis thaliana, Oryza sativa and other angiosperms with B-class genes have AP3 and PI