The origin of land plants: a union of alga and fungus advanced by flavonoids?

Abstract

This paper addresses the hypothesis that land plants have a biphyletic origin as the product of an endocellular mutualism between a green alga and a tip-growing, fungus-like organism, culminating in the acquisition of part of the latter's genome by the host alga (Atsatt, P.R., 1988, Are vascular plants ‘inside-out’ lichens? Ecology 69, 17–23). According to this hypothesis, the tip-growing symbiont's capacity for invasive growth was exploited during the further evolution of the holobiont for the development of various specialized plant cell types, but especially those displaying tip growth. Here, noting the recent discovery of the dependence of pollen tube tip growth on flavonoids, this hypothesis is refined and extended by suggesting that a symbiotic relationship was advanced by the evolution of UV-protective flavonoids in the alga, followed by the evolution of a growth response by the tip-growing symbiont to the presence of those flavonoids, allowing the symbiont to continue to live with the alga in its new, high-light habitat. This growth response then evolved into a dependence on flavonoids in the context of an obligate, mutualistic relationship progressing toward endosymbiosis and incorporation of the endocytobiont's genetic capacity for cell polarization, tip growth and their control into the host alga's genome. Land plants and advanced charophycean algae (which are the closest green-algal relatives of land plants) are likely products of this process, while a primitive charophycean alga (lacking both tip growth and cell polarization) is proposed to have been the likely host for the endocytobiont. A series of tests of this hypothesis, based mainly on the identification and molecular phylogenetic analysis of appropriate genes, are proposed. Whether the endocytobiont could have been a relative of the earliest endomycorrhizal fungi is assessed.