Widespread impact of horizontal gene transfer on plant colonization of land

Abstract

In complex multicellular eukaryotes such as animals and plants, horizontal gene transfer is commonly considered rare with very limited evolutionary significance. Here we show that horizontal gene transfer is a dynamic process occurring frequently in the early evolution of land plants. Our genome analyses of the moss Physcomitrella patens identified 57 families of nuclear genes that were acquired from prokaryotes, fungi or viruses. Many of these gene families were transferred to the ancestors of green or land plants. Available experimental evidence shows that these anciently acquired genes are involved in some essential or plant-specific activities such as xylem formation, plant defence, nitrogen recycling as well as the biosynthesis of starch, polyamines, hormones and glutathione. These findings suggest that horizontal gene transfer had a critical role in the transition of plants from aquatic to terrestrial environments. On the basis of these findings, we propose a model of horizontal gene transfer mechanism in nonvascular and seedless vascular plants.

Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

“…In plants, the horizontal acquisition of genes from microbial sources has been hypothesized to play an important role in early land plant evolution (9). HGT among plant lineages may also occur; a notable example involves the adaptive transfer of a photoreceptor gene from bryophytes that enabled ferns to adapt to low-light conditions (10).…”

Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants

“…The shared ability to bind with PSI might be derived from their common ancestral LHC protein present in the earlier green algal lineage, which evolved into CrLhcbm5 in the succeeding C. reinhardtii, while the one horizontally transferred to the early moss lineage evolved into Lhcb9 in P. patens. As HGT is essential for the transition during plant terrestrialization [29], it is hypothesized that the Lhcb9-mediated, larger PSI-LHCI supercomplex might have promoted survival under certain environmental conditions for the ancestral lineage of mosses [25 ].…”

The evolution of land plants: a perspective from horizontal gene transfer

“…Compared with aquatic environments, terrestrial habitats brought many challenges to early land plants (e.g., desiccation, UV radiation, and microbial attack). During their colonization of land, plants evolved some complex regulatory systems, body plans, and other phenotypic novelties that facilitated their adaptation and radiation in a hostile terrestrial environment [32,33]. The origin and evolution of these novelties were aided through acquisition of genes from other organisms [32][33][34].…”

“…Given the role of lignin in xylem formation and flavonoids in protecting plants from microbial infection and/or UV radiation, the acquisition of PAL might have been crucial for plant adaptation to terrestrial environments. A more comprehensive genome analysis of the moss Physcomitrella patens identified 57 gene families that were transferred from prokaryotes, fungi or viruses to the most recent common ancestors of land plants or green plants [33]. These genes are involved in some essential or plant-specific activities such as xylem formation, plant defense or nitrogen recycling [33,34].…”