Sugar Treatments Can Induce AcLEAFY COTYLEDON1 Expression and Trigger the Accumulation of Storage Products during Prothallus Development of Adiantum capillus-veneris

Abstract

A seed is an intricate structure. Of the two development processes involved in seed formation, seed maturation, or seed program includes accumulation of storage products, acquisition of desiccation tolerance, and induction of dormancy. Little is known about how these processes were originated and integrated into the life cycle of seed plants. While previous investigation on seed origin was almost exclusively through fossil comparison in paleobotany, a wealth of information about the key role of LEAFY COTYLEDON1 (LEC1) in seed formation of spermatophyte inspired a new approach to investigating the seed origin mystery. Here, we examined the expression pattern of AcLEC1 during the entire life cycle of Adiantum capillus-veneris, a non-seed plant, confirmed no AcLEC1 gene expression detectable in prothalli, demonstrated inductive expressed by both sucrose and glucose in prothalli. As expected, we found that sugar treatments delayed prothallus development, promoted differentiation of reproductive organs, and triggered accumulation of storage products. These findings demonstrated links between the sugar treatments and the induction of AcLEC1 expression, as well as the sugar treatments and the events such as accumulation of storage products, which is similar to those considered as seed maturation process in seed plants. These links support a modified hypothesis that inductive expression of LEC1 homologs during embryogenesis might be a key innovation for the origin of the seed program.

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 ).…”

Origins of the seed: The “golden-trio hypothesis”

“…While no LEC1 -like sequences were found the genomes of algae and bryophytes, LEC1 -like sequences were present in the lycophyte Selaginella (highlighted in Figure 5A ), as well as in other lycophyte and fern genomes ( Xie et al, 2008 ). Gene expression and genetic complementation analyses excluded the possibility that the LEC1 -like sequences identified in the pteridophytes are pseudogenes ( Figure 5B ) and demonstrated that the LEC1 -like sequences are expressed under stress conditions ( Figure 5C ; Fang et al, 2017 ; Li et al, 2017 ).…”

“…Not only could its gametophytic development be manipulated under laboratory conditions, but its representative gene expression and metabolite accumulation were also possible to analyze during gametophytic development. Using such an experimental system, Fang et al (2017) showed that sugar treatments can induce Adiantum capillus-veneris LEAFY COTYLEDON1 ( AcLEC1 ) expression and trigger the accumulation of storage products during prothallus (gametophyte) development. While it remains to be determined whether the sugar treatments directly caused the increase in AcLEC1 expression and the accumulation of storage products, these findings provided the first supporting evidence for the golden-trio hypothesis.…”

“…Current information suggests that a lack of downstream genes is less likely the reason for no seed program in pteridophytes (Han et al, 2017;Li et al, 2017). As for the second possibility, while stress-induced expression of LEC1-like genes was found during sporophytic development in both Selaginella and Adiantum, none was detected during gametophytic development (Fang et al, 2017). As gametophytic development is highly sensitive to dehydration and ABA application, it is necessary to find other conditions to test whether LEC1-like genes can be expressed during gametophytic development.…”