Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms

Abstract

Plant MADS-box genes form a large gene family for transcription factors and are involved in various aspects of developmental processes, including flower development. They are known to be subject to birth-and-death evolution, but the detailed features of this mode of evolution remain unclear. To have a deeper insight into the evolutionary pattern of this gene family, we enumerated all available functional and nonfunctional (pseudogene) MADS-box genes from the Arabidopsis and rice genomes. Plant MADS-box genes can be classified into types I and II genes on the basis of phylogenetic analysis. Conducting extensive homology search and phylogenetic analysis, we found 64 presumed functional and 37 nonfunctional type I genes and 43 presumed functional and 4 nonfunctional type II genes in Arabidopsis. We also found 24 presumed functional and 6 nonfunctional type I genes and 47 presumed functional and 1 nonfunctional type II genes in rice. Our phylogenetic analysis indicated there were at least about four to eight type I genes and approximately 15-20 type II genes in the most recent common ancestor of Arabidopsis and rice. It has also been suggested that type I genes have experienced a higher rate of birth-and-death evolution than type II genes in angiosperms. Furthermore, the higher rate of birth-and-death evolution in type I genes appeared partly due to a higher frequency of segmental gene duplication and weaker purifying selection in type I than in type II genes.

Fig. 1.

Domain structures of types I and II MADS-box genes in plants and animals. Adapted from ref. on the structures of types I and II genes and from ref. on the structures of MIKC^c-type and MIKC*-type genes.

Fig. 2.

Phylogenetic tree of 79 MIKC-type (type II) genes from Arabidopsis, rice, mosses, and clubmosses. This tree was constructed by the neighbor-joining method with Poisson-correction (PC) distance. One hundred five amino acids were used after all alignment gaps were eliminated. The number for each interior branch is the percent bootstrap value (500 resamplings), and only values >50% are shown. The scale bar indicates the number of amino acid substitutions per site. We generally followed ref. on the notations of Arabidopsis genes. Simplified class names following ref. were used except for classes A, B-AP3, B-PI, C/D, E, FLC, and S. The genes marked with (U) are unassigned genes for any classes. The three numbers in parentheses below each class name refer to the numbers of ancestral MADS-box genes, MADS-box genes in Arabidopsis, and MADS-box genes in rice, respectively. Two MIKC*-type genes (PPM3 and PPM4) from the moss Physcomitrella patens (10) and one MIKC*-type gene (LAMB1) from the clubmoss Lycopodium annotinum (8) were used as reference sequences.

Fig. 3.

Phylogenetic tree of 223 M-domain sequences from Arabidopsis, rice, mosses, clubmosses, and animals. This tree was constructed by the neighbor-joining method with p-distance and the pairwise deletion option (29) of ≈55 aa. p-distance is known to be more efficient in obtaining the correct topology when the sequence length is short (42). The genes from Arabidopsis and rice are labeled with “a” and “r,” respectively. The reference sequences from the moss P. patens and the clubmoss L. annotinum are labeled with “m” and “c,” respectively. Genes labeled with black squares (▪) are pseudogenes from Arabidopsis, and those with open squares (□) are pseudogenes from rice. Interior branches with bootstrap values (500 bootstraps) >50% are indicated by black dots (•). The portion of the tree corresponding to the MIKC^c-type genes is compressed, because it is essentially the same as that in Fig. 2. The numbers in parentheses below each class name are the numbers of ancestral MADS-box genes, MADS-box genes in Arabidopsis, and MADS-box genes in rice, in this order.

Fig. 4.

Genomic organization of MADS-box genes in Arabidopsis. Genes with black dots (•) are pseudogenes. For seven annotated pseudogenes, we used their gene codes from GenBank. Unannotated pseudogenes are indicated by “p” in front of the name of the functional gene that is most similar to the pseudogene. For example, a pseudogene that is most similar to “SVP” is designated as “pSVP.” The class name of each gene is given in parentheses at the end of the gene name. Of these class names, “(α),” “(β),” “(γ),” and “(U)” refer to “Mα,” “Mβ,” “Mγ,” and “Unassigned,” respectively. I, II, III, IV, and V represent chromosome numbers. The scale bar below chromosome II is for 2 megabase pairs (Mb).