Growth from two transient apical initials in the meristem ofSelaginella kraussiana

Abstract

A major transition in land plant evolution was from growth in water to growth on land. This transition necessitated major morphological innovations that were accompanied by the development of three-dimensional apical growth. In extant land plants, shoot growth occurs from groups of cells at the apex known as meristems. In different land plant lineages, meristems function in different ways to produce distinct plant morphologies, yet our understanding of the developmental basis of meristem function is limited to the most recently diverged angiosperms. To redress this balance, we have examined meristem function in the lycophyte Selaginella kraussiana. Using a clonal analysis, we show that S. kraussiana shoots are derived from the activity of two short-lived apical initials that facilitate the formation of four axes of symmetry in the shoot. Leaves are initiated from just two epidermal cells, and the mediolateral leaf axis is the first to be established. This pattern of development differs from that seen in flowering plants. These differences are discussed in the context of the development and evolution of diverse land plant forms.

Diversity of phyllotaxis in land plants in reference to the shoot apical meristem structure

“…In sporophytes, which are predominant generation, one to two AC forming regularly segmented shoot meristems are present in the Selaginellales [17][18][19][20], whereas the Lycopodiales have multiple superficial initial cells (Fig. 2e) [19,21,22], with four transient initial cells having been reported [23].…”

“…In Isoëtales, the SAM contains one (or two) AC or, alternatively, one group of superficial initials [17,19,24], depending on the age of the plant [25]. Unique to the lycophytes is the presence of microphylls, an evolutionary distinct type of leaf [16,19,24,26] that is initiated by one or two superficial cells in the peripheral zone of the meristem [18,22,27]. In Selaginella, in the SAM with distinct AC, microphylls develop in derivative segments with no particular correlation to the segmentation pattern [28].…”

“…In Selaginella, in the SAM with distinct AC, microphylls develop in derivative segments with no particular correlation to the segmentation pattern [28]. For those species with two functioning ACs, each sagittal sector of the stem is generated by a separate initial cell, and thus, microphylls in these sectors are clonally related to different ACs [18].…”

Sector analysis and predictive modelling reveal iterative shoot-like development in fern fronds

“…The finding that fern fronds have inherent shoot-like properties is consistent with this suggestion. If we assume that the bifurcating stems of extant lycophytes and ferns are similar to the dichotomizing leafless axes of early land plants, then the dichotomy was established following the division of a single shoot apical initial into two identical daughter initials (Bierhorst, 1977;Harrison et al, 2007;Jones and Drinnan, 2009). This scenario allows for evolutionary progression to the formation of fronds if instead of dividing equally, the shoot apical initial divides to renew the shoot apical initial and to generate a daughter with modified developmental potential (the frond apical initial).…”

“…Iterative shoot development has been reported across the land plants, in both haploid gametophyte and diploid sporophyte generations. For example, a single apical initial generates repeating 'leaf' units in Physcomitrella patens gametophytes (Harrison et al, 2009), and in the lycophyte Selaginella kraussiana, one or two apical initials generate repeating units of leaf pairs along the bifurcating sporophyte stem (Harrison and Langdale, 2010;Harrison et al, 2007;Jones and Drinnan, 2009). In seed plants, iterative shoot development involves the repeated production of phytomer units from multicellular apical meristems (for a review, see Steeves and Sussex, 1989).…”