Does integument arise de novo or from pre-existing structures? ── Insights from the key regulatory genes controlling integument development

Abstract

The origin of seeds is one of the key innovations in land plant evolution. Ovules are the developmental precursors of seeds. The integument is the envelope structure surrounding the nucellus within the ovule and developing into the seed coat when ovules mature upon fertilization. The question of whether the integument arise de novo or evolve from elaboration of pre-existing structures has caused much debate. By exploring the origin and evolution of the key regulatory genes controlling integument development and their functions during both individual and historical developmental processes, we showed the widespread presence of the homologs of ANT, CUC, BEL1, SPL, C3HDZ, INO, ATS, and ETT in seedless plant genomes. All of these genes have undergone duplication-divergence events in their evolutionary history, with most of the descendant paralogous suffering motif gain and/or loss in the coding regions. Expression and functional characterization have shown that these genes are key components of the genetic program that patterns leaf-like lateral organs. Serial homology can thus be postulated between integuments and other lateral organs in terms of the shared master regulatory genes. Given that the genetic program patterning leaf-like lateral organs formed in seedless plants, and was reused during seed origin, the integument is unlikely to arise de novo but evolved from the stem segment-specific modification of pre-existing serially homologous structures. The master ‘switches’ trigging the modification to specify the integument identity remain unclear. We propose a successive transformation model of integument origin.

Evolution of the WRKY66 Gene Family and Its Mutations Generated by the CRISPR/Cas9 System Increase the Sensitivity to Salt Stress in Arabidopsis

“…The ancestral genes of the WRKY66 homologs had been duplicated in angiosperm genomes, prior to the radiation of extent flowering plants. Strictly speaking, the WRKY66 orthologs were angiosperm-specific because they were all derived from the angiosperm-specific duplication events ( Figure 1 B), similar to the divergence pattern of the PIF , BEL1 and ANT [ 38 , 39 ]. Then, the whole genome duplication giving rise to modern angiosperms [ 40 ], together with additional tandem duplications [ 41 ], thus created the genetic substrate for the structural and functional diversification of genes.…”

Evolutionary studies of the basic helix–loop–helix (bHLH) IVc gene family in plants and the role of AtILR3 in Arabidopsis response to ABA stress

“…Following the duplication, the first early expansion happened before the divergence of lycophytes, resulting in the occurrence of Clade B (ILR3_L linage) and other Clades. It was noteworthy that the Clade B ILR3s only existed in pteridophyte and gymnosperm genome, implying that their evolutionary intermediates probably did not survive, or their evolution was intercepted due to some reasons in angiosperms, which was similar to the situations of C3HDZ genes (Jiang et al, 2023). Afterwards, the second expansion occurred before the divergence of angiosperms, resulting in the establishment of ILR3 , IDT1 , and bHLH34_115 lineages (Figure 2B and Figure 3), exposing distinct functional redundancy.…”

“…However, whether it is a conserved function in gymnosperms or even non‐seed plants is unknown. The evolutionary history analysis of plant gene families provides clues about domain organization, expansion mechanism, functional evolution, and so on (Mohanta et al, 2015; Jiang et al, 2023). Since gene duplication is considered to be an important mechanism of functional evolution besides mutation, it offers novel chances and fundamental sources for evolutionary success (Van de Peer et al, 2009), of which whole genome duplications (WGDs) are a crucial evolutionary characteristic (Jiao et al, 2011; Qiao et al, 2019).…”