How was apical growth regulated in the ancestral land plant? Insights from the development of non-seed plants

Abstract

Land plant life cycles are separated into distinct haploid gametophyte and diploid sporophyte stages. Indeterminate apical growth evolved independently in bryophyte (moss, liverwort, and hornwort) and fern gametophytes, and tracheophyte (vascular plant) sporophytes. The extent to which apical growth in tracheophytes co-opted conserved gametophytic gene networks, or exploited ancestral sporophytic networks, is a long-standing question in plant evolution. The recent phylogenetic confirmation of bryophytes and tracheophytes as sister groups has led to a reassessment of the nature of the ancestral land plant. Here, we review developmental genetic studies of apical regulators and speculate on their likely evolutionary history.

Figure 1

Phylogenetic relationships and representative meristem structure of land plants. Bryophyte gametophytes grow as thalli, leafy shoots or filaments, and meristems comprise a single apical cell. Monilophytes also produce thallus-type gametophytes with a notch meristem (in the case of Ceratopteris hermaphrodite gametophytes). Hornwort sporophytes grow from a persistent basal meristem, moss sporophytes grow initially from an apical initial, and subsequently from an intercalary meristem; the mechanism of proliferative growth in liverwort sporophytes appears to be intercalary meristem-like. Selaginella (lycophyte) and Ceratopteris (monilophyte) apices usually have two and one apical initials, respectively, but other lycophytes and monilophytes have apices with multiple initials. Spermatophyte (seed plant) apices are multicellular and functionally more complex. Figure adapted from Harrison (2017).

Figure 2

Putative apical regulators in the ancestral sporophyte. Hypothetical ancestral sporophyte based on extant Physcomitrium morphology. Putative roles inferred from bryophyte gene function that are broadly conserved in vascular plants. In zygotes, WOX and LFY genes are required for the first cell division and KNOX genes promote establishment of the sporophyte (Tanahashi et al., 2005; Sakakibara et al., 2013, 2014; Dierschke et al., 2021). In sporophytes, PpLFY genes are expressed throughout development and Pplfy mutants have disrupted cell division planes in apical and basal regions (Tanahashi et al., 2005); Class I KNOX genes regulate cell division in the apical initial and intercalary meristem, their role in the intercalary meristem is dependent on cytokinin signaling (Sakakibara et al., 2008; Coudert et al., 2019); putative roles for HD-ZIP III and WOX genes in apical initial proliferation are based on gene expression patterns rather than functional data (indicated by white lettering) (Sakakibara et al., 2014; Yip et al., 2016); maintenance of an auxin minimum in the apical initial by basipetal auxin transport promotes stem cell identity (Fujita et al., 2008; Bennett et al., 2014b; Thelander et al., 2019; Nemec Venza et al., 2022); Class II TCP genes repress branching in the proliferative zone (Ortiz-Ramírez et al., 2016).