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) MADSbox genes from the Arabidopsis and rice genomes. Plant MADSbox 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 Ϸ15-20 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. M orphological͞physiological evolution of organisms has been driven mainly by the evolution of genetic toolkits for developmental͞physiological processes such as transcription factors and signaling pathways (1). A large proportion of genetic toolkits are highly conserved even between distantly related organisms. In flowering plants (angiosperms), MADS-box genes are among such toolkits that control various aspects of developmental processes. MADS-box genes are defined by the highly conserved 180-bp-long motif called the MADS-box and are found in animals, fungi, and plants (2). The protein region encoded by the MADS-box is called the MADS-domain (or Mdomain) and is part of the DNA-binding domain. It has been proposed that there are at least two evolutionary lineages (types I and II) of MADS-box genes in animals, fungi, and plants (3) (Fig. 1).There are Ϸ100 MADS-box genes in Arabidopsis thaliana (hereafter called Arabidopsis) and Ͼ70 MADS-box genes in Oryza sativa (hereafter called rice). There are Ϸ40 clearly identifiable type II MADS-box genes in each of Arabidopsis (4, 5) and rice (6). Most of the plant type II genes contain three additional plant-specific domains: intervening (I) domain (Ϸ30 codons), keratin-like coiled-coil (K) domain (Ϸ70 codons), and C-terminal (C) domain (variable length) (7) (Fig. 1). These genes are called MIKC-type genes. The MIKC-type genes can further be divided into two types based on the intron-exon structure: MIKC c -and MIKC*-type genes (8). The MIKC c -type genes have been identified in most major evolutionary lineages of green plants such as...

Gene duplications, robustness and evolutionary innovations

“…Yeast, nematode, and fruit fly genomes contain only between two and four MADS box genes 40,41 ; the most recent common ancestor of gymnosperms and angiosperms may have had as few as 7 MADS box genes 36,42 . In contrast, the two completely sequenced genomes of the angiosperms Arabidopsis thaliana and rice each contain more than 70 MADS box genes 38,39 .…”

“…MADS box proteins are ubiquituous in eukaryotes. Flowering plants have experienced a wave of duplication in these genes [36][37][38][39][40] (Figure 1). Yeast, nematode, and fruit fly genomes contain only between two and four MADS box genes 40,41 ; the most recent common ancestor of gymnosperms and angiosperms may have had as few as 7 MADS box genes 36,42 .…”

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…Type I MADS-box genes show a higher rate of gene birth and death, often due to gene duplication-transposition, than Type II genes (Nam et al, 2004;Freeling et al, 2008;Wang et al, 2016b). Also, the function of the different Type I genes is generally poorly characterized.…”

“…The relationships between the major clades of the plant MADS-box genes have already largely been inferred in various phylogenetic and evolutionary studies (Becker and Theissen, 2003;Martinez-Castilla and Alvarez-Buylla, 2003;Nam et al, 2003Nam et al, , 2004Nam et al, , 2005Gramzow et al, 2012Gramzow et al, , 2014Smaczniak et al, 2012;Ruelens et al, 2013;Sun et al, 2014;Yu et al, 2016b) (Figure 1B). However, these studies cannot fully resolve some of the deepest nodes of the MADS-box gene tree.…”

Genome-Wide Analysis of Basic/Helix-Loop-Helix Transcription Factor Family in Rice and Arabidopsis

“…Our results indicate that the birth rate seemed greater than the death rate in flowering plant bHLH family. Similarly, other large transcription factor families often experience birth-and-death evolution, such as the MADS-box gene family in both rice and Arabidopsis (Nam et al, 2003(Nam et al, , 2004.…”