Morphological evolution in land plants: new designs with old genes

Abstract

The colonization and radiation of multicellular plants on land that started over 470 Ma was one of the defining events in the history of this planet. For the first time, large amounts of primary productivity occurred on the continental surface, paving the way for the evolution of complex terrestrial ecosystems and altering global biogeochemical cycles; increased weathering of continental silicates and organic carbon burial resulted in a 90 per cent reduction in atmospheric carbon dioxide levels. The evolution of plants on land was itself characterized by a series of radical transformations of their body plans that included the formation of three-dimensional tissues, de novo evolution of a multicellular diploid sporophyte generation, evolution of multicellular meristems, and the development of specialized tissues and organ systems such as vasculature, roots, leaves, seeds and flowers. In this review, we discuss the evolution of the genes and developmental mechanisms that drove the explosion of plant morphologies on land. Recent studies indicate that many of the gene families which control development in extant plants were already present in the earliest land plants. This suggests that the evolution of novel morphologies was to a large degree driven by the reassembly and reuse of pre-existing genetic mechanisms.

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…However, wholesale changes in numbers or types of protein families and domain structures need not underlie the innovations required to achieve multicellularity as evidenced by the similarity between the C. reinhardtii and V. carteri genomes , and shared origins with C. reinhardtii of key developmental regulators in V. carteri. Similar ideas have emerged from investigating the origins of developmental pathways from land plants that arose in charophyte algae or the earliest embryophyte lineages (Preston et al 2011;Pires and Dolan 2012;Bowman 2013). Third, lineage-specific protein families such as the Chlamydomonas cell wall/Volvox ECM proteins may provide a particularly rich source of raw material for evolutionary innovation.…”

“…Although data are incomplete, some progress has been made in identifying charophyte algal homologs of key developmental regulators used by embryophytes Pires and Dolan 2012;Bowman 2013). Without complete genome sequences this list is relatively short and incomplete, but provides a sample of potential discoveries that might be made with increased knowledge of charophyte algal genomes and developmental patterning mechanisms.…”

Atmospheric carbon dioxide: a driver of photosynthetic eukaryote evolution for over a billion years?

“…The evolutionary appearance of land plants marked emergence of the terrestrial biosphere, and Pires & Dolan [18] synthesize recent advances in evolutionary developmental biology that shed light on how plant body plans and morphology diversified during their successful colonization of terrestrial environments. They conclude that the core genetic toolkits of distantly related plants are remarkably similar, and that the evolution of form derives from altered expression patterns of ancient lineages of regulatory genes throughout land plant evolution.…”

Seed evolution: parental conflicts in a multi-generational household

“…Even in derived and complex charophytes, such as Coleochaete (where egg cells are enveloped and protected by a layer of gametophytic cells) the fertilized zygote directly undergoes meiosis to form free-dispersing haploid spores (1). One of the crucial innovations of the first land plants was an intercalation of mitotic divisions in the zygote before meiosis, causing the development of a multicellular embryo (a young sporophyte) within gametophytic tissue (2,3). The sheltered multicellular sporophyte increased the number of spores that could be produced from a single water-dependent fertilization event, offering a huge competitive advantage on land.…”