The evolution of the shoot apical meristem from a gene expression perspective

‘A long-standing question in plant evolution is whether the complex meristems of angiosperms were derived from the simple meristems of these early-diverging lineages, or were simple meristems derived from more complex meristems.’ Ferns (monilophytes) and some lycophytes, including Selaginella moellendorffii, have apical meristems that are unusual compared to the apical meristems of angiosperms. Fern and Selaginella apical meristems have a single distinct apical, pie-shaped cell whereas the angiosperm meristem is multicellular with distinct zones and layers and no apical cell (Fig. 1). Given that lycophytes and monilophytes (collectively referred to as pteridophytes) diverged early in land plant evolution 300–400 million years ago and before the divergence of seed plants, a long-standing question in plant evolution is whether the complex meristems of angiosperms were derived from the simple meristems of these early-diverging lineages, or were simple meristems derived from more complex meristems. The former hypothesis is supported by the occurrence of an apical cell in the meristems of early-diverging lycophyte and monilophyte lineages, suggesting that the apical cell is a plesiomorphic trait. The argument favoring the latter hinges on the lycophyte Lycopodium (now referred to as Huperzia), which lacks the distinct apical cell observed in Selaginella. Molecular phylogenies (Qiu et al., 2007; Karol et al., 2010) suggest that the Selaginellales are derived from a lineage that now includes the Lycopodiales; in the lycophyte lineage, the apical cell is, therefore, a derived trait. The study by Frank et al. is the first to move beyond histological comparisons of meristems and has employed RNA-seq to define the differences in apical meristems across vascular plants at the transcription level. Using laser microdissection, different domains (Fig. 1) of the meristems of maize, Equisetum arvense (a monilophyte) and Selaginella moellendorffii were isolated and collected. RNA-seq was then used to catalog the transcripts within each of the domains and differentially expressed genes identified. In this study, differential gene expression was determined by comparing the abundance of transcripts in each meristem domain to the abundance of transcripts in whole-plant samples of the same species. One striking finding from the study by Frank et al. is that the apical cell and the meristem core (Fig. 1) of each pteridophyte is transcriptionally distinct (and especially so in Selaginella), as is the apical meristem and P1 region of the shoot meristem of maize. In situ hybridizations in Selaginella of a homeodomain transcription factor and a PIN1 auxin efflux carrier, which are up-regulated in the apical cells of Selaginella and Equisetum, revealed that while the homeodomain transcription factor localizes to the apical cell as expected, PIN1 transcripts accumulate in a ring around the apical cell. The expression pattern of PIN1 is similar to that observed in the angiosperm root, leading the authors to speculate that their data supports the long-held hypothesis (reviewed in Banks, 2009) that the Selaginella root and shoot identities are functionally similar. It will be interesting to see if similar patterns of PIN1 expression, plus additional shoot meristem genes, are also observed in the apical meristem of the Selaginella root. How similar are the meristems of Selaginella and Equistem from a gene expression perspective? According to Frank et al.'s study, the answer is not very. Less than 10% of the apical cell differentially expressed genes are shared between these two plants, and only c. 1% of the meristem core differentially expressed genes are shared. However, in pairwise comparisons of differentially expressed genes in the apical cells of Selaginella and Equistem to the maize meristem, a larger number of genes (22% and 31%, respectively) are shared. These shared genes include a list of those known to be involved in different aspects of meristem function in angiosperms. Although the study by Frank et al. does not cleanly resolve the question of who came first, the simple apical-cell-type meristem or the multicellular, no-apical-cell-type meristem, it does support the concept that the simple pteridophyte meristem, like the more complex meristems of angiosperms, is organized into distinct zones. While the meristems of the two pteridophytes examined are transcriptionally distinct, they also share a set of core genes that may carry out the essential functions of the meristem. Given the success of the LC-RNA-seq approach, examining additional lycophytes and monilophyte species should reveal how similar the apical meristems within each lineage are at the transcription level. This approach combined with the recent development of a method to efficiently transform the fern Ceratopteris richardii (Plackett et al., 2014) make Ceratopteris an ideal species to examine the biological functions of these genes.