Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene

Abstract

Heterostyly represents a fascinating adaptation to promote outbreeding in plants that evolved multiple times independently. While l-morph individuals form flowers with long styles, short anthers, and small pollen grains, S-morph individuals have flowers with short styles, long anthers, and large pollen grains. The difference between the morphs is controlled by an S-locus “supergene” consisting of several distinct genes that determine different traits of the syndrome and are held together, because recombination between them is suppressed. In Primula, the S locus is a roughly 300-kb hemizygous region containing five predicted genes. However, with one exception, their roles remain unclear, as does the evolutionary buildup of the S locus. Here we demonstrate that the MADS-box GLOBOSA2 (GLO2) gene at the S locus determines anther position. In Primula forbesii S-morph plants, GLO2 promotes growth by cell expansion in the fused tube of petals and stamen filaments beneath the anther insertion point; by contrast, neither pollen size nor male incompatibility is affected by GLO2 activity. The paralogue GLO1, from which GLO2 arose by duplication, has maintained the ancestral B-class function in specifying petal and stamen identity, indicating that GLO2 underwent neofunctionalization, likely at the level of the encoded protein. Genetic mapping and phylogenetic analysis indicate that the duplications giving rise to the style-length-determining gene CYP734A50 and to GLO2 occurred sequentially, with the CYP734A50 duplication likely the first. Together these results provide the most detailed insight into the assembly of a plant supergene yet and have important implications for the evolution of heterostyly.

The Turnera Style S-Locus Gene TsBAHD Possesses Brassinosteroid-Inactivating Activity When Expressed in Arabidopsis thaliana

“…In Primula , five genes have been identified within the S -locus: CYP734A50 (a cytochrome p450), GLOBOSA2 ( GLO2 , a MADS box transcription factor), PUM (a Pumilio-like RNA-binding protein), CCM (a cyclin-like F box gene), and KFB (a Kelch repeat F box protein) [ 10 , 12 , 13 , 14 , 15 ]. CYP734A50 is a member of the P450 CYP734A cytochrome family expressed in pistils [ 13 ].…”

“…This observation led to an elegant set of experiments that demonstrated that Primula CYP734A50 controls pistil length in the S-morph by reducing cell expansion by degrading BRs [ 13 ]. GLOBOSA2 ( GLO2) is a MADS-box transcription factor expressed specifically in S-morph stamens [ 10 , 12 , 15 ], and was recently shown to control (elevate) anther height by promoting cell expansion in the corolla tube below the point of anther filament insertion [ 14 ]. The potential functions of the other three Primula S -genes are as yet unknown.…”

Evolutionary Divergence and Biased Expression of NAC Transcription Factors in Hexaploid Bread Wheat (Triticum aestivum L.)

“…In addition, the duplicate genes usually have divergent functions [ 49 ]. Neofunctionalization supports the notion that one gene maintains the ancestral function while the other gets new functions after duplication [ 50 ], and neofunctionalization is an important impetus for plant evolution [ 27 ]. The event of neofunctionalization had been detected in wheat and supposed to contribute to the adaptation of wheat to a diversity of conditions [ 25 , 26 ].…”

“…Similar expressed pattern of homologous NAC transcription factors was observed in durum wheat and bread wheat [ 22 , 23 ]. Due to the importance of functional divergence for plant evolution [ 27 ] and the important functions of TaNACs, we focused on the biased expression of TaNACs to understand the TaNAC evolution. By comparing the expression pattern of each TaNAC in one group, it was found that neofunctionalization was one of the important ways, whether under biotic stress or abiotic stress.…”

“…However, the divergent functions of orthologous and homologous genes in poaceae plants were also observed by researchers [ 24 , 25 , 26 ]. In addition, the event of functional divergence was supposed to be an important impetus for plant evolution [ 27 ].…”