Characterization of Two AGL6–Like Genes from a Chinese Endemic Woody Tree, Manglietia patungensis (Magnoliaceae) Provides Insight into Perianth Development and Evolution in Basal Angiosperms

Zhixiong Liu,Kebin Zhang,Faju Chen,Yue Fei,Laiyun Li

doi:10.3390/f10080669

Abstract

Manglietia patungensis (Magnoliaceae) exhibits radially symmetric flowers with perianth consisting of three separate sepaloid tepals in whorl 1 and six petaloid tepals in the inner two whorls, which shows an obvious difference from flowers of most Magnoliaceae species that contain three uniform petaloid tepals whorls, and make it an excellent model for understanding perianth morphology differentiation during early flower evolution. Here, two AGL6 orthologs, MapaAGL6-1 and MapaAGL6-2, were isolated from M. patungensis. Sequence alignment and phylogenetic analyses grouped both genes into the AGL6 lineage. MapaAGL6-1 is expressed only in the perianth whorls, while MapaAGL6-2 is strongly expressed in the perianth whorls but is lowly expressed in gynoecium. Furthermore, ectopic expression of MapaAGL6-1 results in strong complementation phenotypes in the Arabidopsis ap1-10 flower and production of normal floral organs in four floral whorls only with the petal number reduced in whorl 2, while ectopic expression of MapaAGL6-2 only results in petals partly rescued but failing to terminate carpelloid development in Arabidopsis ap1-10 mutant. In addition, the daughter lines generated from a cross between 35S::MapaAGL6-1 transgenic plants showing strong phenotypes and 35S::MapaAGL6-2 transgenic plants showing phenotypic changes produce normal flowers. Our results suggest that MapaAGL6-1 is a reasonable A-function gene controlling perianth identity in Magnoliaceae, which infers from its expression region and complementation phenotypes in Arabidopsis ap1 mutant, while MapaAGL6-2 is mainly involved in petaloid tepal development. Our data also provide a new clue to uncover the perianth development and early evolution in basal angiosperms.

Highlights

The long-established ABCE model has provided a detailed picture of how perfect floral organs are formed in the core eudicot model systems Arabidopsis and Antirrhinum [1,2,3]
Deduced proteins alignment and a phylogenetic tree grouped both the MapaAGL6-1 and MapaAGL6-2 into AGL6 lineage (Figure 2). Both genes were designated as MapaAGL6-1 (Manglietia patungensis AGAMOUS-like 6)
Perianth is widely present in almost all extant angiosperms and a double perianth with sepals and petals differentiated is considered to be a key innovation for eudicots [29]

Summary

Introduction

The long-established ABCE model has provided a detailed picture of how perfect floral organs are formed in the core eudicot model systems Arabidopsis and Antirrhinum [1,2,3]. The expressions of A-function genes are restricted to the first and second whorls for specifying perianth (sepal and petal) identity by the C-class genes [3,4]. APETALA1 (AP1) and AP2 reportedly confer A function in Arabidopsis. The AP1 ortholog from Antirrhinum, SQUAMOSA (SQUA), does not have A-function, the AP2 homologs, LIPLESS1 (LIP1) and LIP2, confer partial A-function by contributing to perianth identity [5]. Previous study has suggested that the A-function for AP1 may be derived in Arabidopsis and perhaps relative species in the rosid clade, but this function has not yet been demonstrated in any species other than Arabidopsis [6].

Methods

Results

Conclusion