Are Vascular Plants "Inside‐Out" Lichens?

This essay considers the possibility that vascular plants originated from an algal-fungal mutualism. Among land plants, the vascular forms are in many ways extraordinary; they seem to be far more than simple evolutionary "extensions" of green algae. They are comparatively too complex, and they diversified too quickly. More important, they contain numerous overtly funguslike cells. It is primarily this observation that leads me to speculate that these elaborate organisms are the genetic legacy of both algal and fungal ancestors. We can reasonably assume that the fungi have an ancient history of intimate association with the algae (Ahmadjian 1987) and were probably involved in the original transition to land. First Jeffrey (1962) and then Pirozynski and Malloch (1975) hypothesized that all terrestrial plants arose from an ancient symbiosis between a semiaquatic ancestral green alga and an aquatic fungus, an oomycete. The essence of this important proposal, elaborated by Pirozynski and Malloch, is that land plants are "reverse-phase" lichens in which the alga evolved into the dominant component and the fungus became a mineral-scavenging endophyte, much as we see today in extant mycorrhizal associations. Indeed, this alga-dominant prototype is reflected in many marine associations called "mycophycobioses" (Ahmadjian and Paracer 1986). The merger I will propose came much later but prior to the evolution of vascular tissue, perhaps in a close ancestor of the Rhyniophyta, but probably in a more Coleochaete-like organism (Bold et al. 1987). It began with fungal parasitism, may have evolved into a mutualism, and culminated in the acquisition of the fungal genome by the plant host. My story is in accord with mounting evidence that parasites can rapidly become required cellular components (Jeon 1987) and have provided the genetic substrate for evolutionary innovations in many types of host populations (Price et al. 1986). In this essay, I will argue that vascular plants may in fact be lichenlike chimeras that have genetically internalized their fungal partners. W. F. Lamboy (1984) has developed a somewhat similar albeit less encompassing view. Lamboy suggests that some of the evolution that has taken place in the angiosperms (and other plant groups) is attributable to horizontal gene transfer (hgt) from parasitic or symbiotic fungi to their flowering-plant hosts. He describes three conditions necessary for fungus-to-angiosperm hgt and suggests that all can be satisfied by normal fungus-angiosperm interactions: (1) the fungus must be in intimate contact with the host's reproductive cells or the meristematic cells that give rise to these structures; (2) physical barriers to DNA transfer must be overcome; and (3) the transferred DNA must become incorporated into the genome of the host's reproductive cells. As one example of the kind of trait that could have resulted from hgt, Lamboy suggests that corn evolved from teosinte by hgt from the fungus Ustilago maydis, which could have provided the genes responsible for sex change and dwarfing of the teosinte tassel. Although hgt is a reasonable mechanism for the acquisition of fungal genes, this process is too "piecemeal" to give vascular plants the kinds of genetic endowment that I visualize.