Evolutionary Analysis of the LAFL Genes Involved in the Land Plant Seed Maturation Program

Abstract

Seeds are one of the most significant innovations in the land plant lineage, critical to the diversification and adaptation of plants to terrestrial environments. From perspective of seed evo-devo, the most crucial developmental stage in this innovation is seed maturation, which includes accumulation of storage reserves, acquisition of desiccation tolerance, and induction of dormancy. Based on previous studies of seed development in the model plant Arabidopsis thaliana, seed maturation is mainly controlled by the LAFL regulatory network, which includes LEAFY COTYLEDON1 (LEC1) and LEC1-LIKE (L1L) of the NF-YB gene family, and ABSCISIC ACID INSENSITIVE3 (ABI3), FUSCA3 (FUS3), and LEC2 (LEAFY COTYLEDON2) of the B3-AFL gene family. In the present study, molecular evolution of these LAFL genes was analyzed, using representative species from across the major plant lineages. Additionally, to elucidate the molecular mechanisms of the seed maturation program, co-expression pattern analyses of LAFL genes were conducted across vascular plants. The results show that the origin of AFL gene family dates back to a common ancestor of bryophytes and vascular plants, while LEC1-type genes are only found in vascular plants. LAFL genes of vascular plants likely specify their co-expression in two different developmental phrases, spore and seed maturation, respectively, and expression patterns vary slightly across the major vascular plants lineages. All the information presented in this study will provide insights into the origin and diversification of seed plants.

Central role of the LEAFY COTYLEDON1 transcription factor in seed development

“…The requirement of LEC1 to regulate maturation processes opens the possibility that LEC1 may have played a critical role in the evolution of the maturation phase and the seed habit. Consistent with this possibility, phylogenetic analysis revealed that LEC1 ‐type genes, which are shared among all spermatophytes, are first detected among basal land plant lineages in lycophytes (Xie et al ; Kirkbride et al ; Cagliari et al ; Fang et al ; Han et al ), suggesting that LEC1 originated at least 30 million years before the appearance of seed plants in the fossil record. Based on their expression patterns, LEC1 orthologs have been suggested to play roles in promoting desiccation tolerance and lipid accumulation in Selaginella (lycophyte) species and storage macromolecule accumulation in reproductive organs of the fern, Adiantumcapillus‐veneris (Xie et al ; Kirkbride et al ; Fang et al ; Han et al ).…”

Genes, proteins and other networks regulating somatic embryogenesis in plants

“…Embryo identity and maturation are regulated by the network of LAFL proteins LEC1/LEC1-LIKE (L1L), ABSCISIC ACID INSENSITIVE 3 (ABI3), FUSCA3 (FUS3), and (LEC2) where B9 and B3 domains are encoded by LEC1 and LEC2 genes, respectively [ 145 ]. B9 is a subunit of NUCLEAR factor Y (NF-Y-B9), and B3 is a domain which contains transcription factor LEC2 [ 160 ] playing a role in maintaining the morphology of suspensor, progression via maturation phase, cotyledon identity specification, and suppressing premature germination [ 46 ]. Accumulation of storage macromolecules, desiccation tolerance, and cotyledon development are defective in zygotic embryos where loss of function mutation occurs in LAFL genes.…”

Structural variation affecting DNA backbone interactions underlies adaptation of B3 DNA binding domains to constraints imposed by protein architecture

“…ABI3 and VAL1 have complex, multiple domain architectures that physically integrate B3 recognition of the Sph/RY cis-element with hormonal signals (3)and chromatin marks (3,6,7,(11)(12)(13), respectively, whereas LEC2 and FUS3 have architectures of reduced complexity conducive to their roles as pioneer activators (14,15). Orthologs of VP1/ABI3 and VAL1 type proteins occur in all sequenced land plant genomes (16), whereas FUS3 and LEC2 genes are restricted to seed plants and rosid clade of angiosperms, respectively (16). This phylogenetic relationship is consistent with FUS3 and LEC2 proteins having evolved via truncation of VP1/ABI3 type ancestors (15,16).…”

“…Orthologs of VP1/ABI3 and VAL1 type proteins occur in all sequenced land plant genomes (16), whereas FUS3 and LEC2 genes are restricted to seed plants and rosid clade of angiosperms, respectively (16). This phylogenetic relationship is consistent with FUS3 and LEC2 proteins having evolved via truncation of VP1/ABI3 type ancestors (15,16). While the DNA sequence specificities of B3 domains in VAL1 and AFL proteins are conserved, the contributions of intrinsic differences in B3 domain properties to functional diversification in the B3 transcription factor network have not been systematically addressed.…”