The Evolution of euAPETALA2 Genes in Vascular Plants: From Plesiomorphic Roles in Sporangia to Acquired Functions in Ovules and Fruits

Abstract

The field of evolutionary developmental biology (evo-devo) can help address how morphological novelties evolve, a key question in evolutionary biology. In Arabidopsis thaliana, APETALA2 (AP2) plays a role in the development of key plant innovations including seeds, flowers, and fruits. AP2 belongs to the APETALA2/ETHYLENE RESPONSIVE ELEMENT BINDING FACTOR (AP2/ERF) family which has members in all viridiplantae, making it one of the oldest and most diverse gene lineages. One key subclade, present across vascular plants is the euAPETALA2 (euAP2) clade, whose founding member is AP2. We reconstructed the evolution of the euAP2 gene lineage in vascular plants to better understand its impact on the morphological evolution of plants, identifying seven major duplication events. We also performed spatio-temporal expression analyses of euAP2/TOE3 genes focusing on less explored vascular plant lineages, including ferns, gymnosperms, early diverging angiosperms and early diverging eudicots. Altogether, our data suggest that euAP2 genes originally contributed to spore and sporangium development, and were subsequently recruited to ovule, fruit and floral organ development. Finally, euAP2 protein sequences are highly conserved, therefore, changes in the role of euAP2 during development are most likely due to changes in regulatory regions.

Identification of genes differentially expressed between prostrate shoots and erect shoots in the lycophyte Selaginella nipponica using an RNA-seq approach

“…AP2 -like genes can be divided into the euAP2 and the ANT clades, and each clade contains genes from algae; thus, both clades have an origin in the common ancestor of green plants ( Shigyo et al 2006 ; Zumajo-Cardona and Pabon-Mora 2016 ; Kerstens et al 2020 ; Zumajo-Cardona et al 2021 ). In S .…”

“…AP2 -like genes are regulated via transcript degradation and translational repression in flowering plants, and miR172 controls these processes ( Zhu and Helliwell 2011 ). MIR172 originated in ancestral euphyllophytes after they had diverged from lycophytes ( Zumajo-Cardona et al 2021 ), and it can slice AP2 -like transcripts in ferns ( Axtell and Bartel 2005 ). Thus, AP2 -like genes must have functioned in the absence of miR172 regulation in S .…”

Heterochrony and repurposing in the evolution of gymnosperm seed dispersal units

“…While there has been substantial progress in understanding the anatomical, developmental and genetic basis of angiosperm fleshy fruits [ 6 ], much less is known about analogous fleshy structures of multiple origin in gymnosperms [ 7 , 8 ], except for Ginkgo and certain Cycadales [ 9 ]. The idea that a basic genetic toolkit involving MADS box genes may be at play in all seed plant fleshy diaspores is appealing [ 10 , 11 ].…”

SMRT and Illumina RNA-Seq Identifies Potential Candidate Genes Related to the Double Flower Phenotype and Unveils SsAP2 as a Key Regulator of the Double-Flower Trait in Sagittaria sagittifolia

“…Flower organs will exhibit a similar phenotype of double flowers to the ap2 mutant after the overexpression of miR172 with the 35S promoter [22,23]. Unlike the situation in Arabidopsis, the AP2-like gene (LIP1 and LIP2) in Antirrhinum majus only redundantly inhibits the function of flower class B and C genes [24]. Therefore, there are differences in the function of the AP2 gene among different species.…”