Coenocytic Growth Phases in Land Plant Development: A Paleo-Evo-Devo Perspective

Abstract

Premise of research. The evolutionary origin of the seed habit coincided with profound physiological and structural changes associated with underlying developmental patterns. A coenocyte is formed during megagametophyte development in many vascular plants, including some lycophytes and all spermatophytes; this structure compares closely with similar free-nuclear growth phases during embryo development in gymnosperms and endosperm development in angiosperms. Methodology. We review the various free-nuclear growth phases that occur during development of the megaspore and of the ensuing seed of land plants in the context of phylogenies of extant embryophytes and recent studies of the genes that underlie plant development. Pivotal results. Two contrasting types of coenocyte are controlled by different genetic systems: coenocytic growth phases that subsequently become cellularized and contribute to the plant body (type a) and terminally differentiated multinucleate structures such as haustorial suspensor cells (type b). Conclusions. Coding decisions made for coenocytic characters may have contributed to the ongoing instability that characterizes morphological cladistic analyses of land plants. Coenocytic growth phases in lycophytes and spermatophytes probably have independent evolutionary origins. However, the strong similarity between them indicates similar underlying genetic machinery; we hypothesize that this type of growth is controlled by ancient regulatory factors that were recruited during the development of novel structures. Combined with heterospory and endospory, a free-nuclear proembryo likely represented a preadaptive factor that facilitated the evolutionary origin of the seed habit. We highlight a positive correlation between a coenocytic growth phase and increased ovule/seed size in early spermatophytes. In general terms, the relatively derived seed plant lineages—including extant conifers, gnetaleans, and angiosperms—have reverted to a smaller seed size and concomitantly restricted coenocytic growth phases that reflect heterochronic change. A positive correlation between coenocytic growth phases and the absence of a preprophase band indicates that suppression of cytokinesis is a significant aspect of early growth phases in spermatophyte life histories.