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.

Figure 1. Molecular phylogenies of subtilases (a) and vein patterning 1 (VEP1) (b).

Numbers above branches show bootstrap values from maximum likelihood and distance analyses, respectively. Asterisks indicate values <50%.

Figure 2. Multiple sequence alignment (a) and molecular phylogeny (b) of acyl-activating enzymes 18 (AAE18).

Boxed columns indicate the amino-acid residues and indels shared by bacterial and green plant AAE18 sequences. Numbers above branches show bootstrap values from maximum likelihood and distance analyses, respectively. Asterisks indicate values <50%.

Figure 3. A hypothetical scheme of HGT in mosses.

Two entry points for foreign genes into the moss genome are proposed. The first entry point is spore germination and the early stage of gametophyte development. The second entry point is fertilization and the early stage of embryo development. This model is also applicable to other nonvascular plants and seedless vascular plants that have independent gametophytes. DNA acquired from foreign sources through the two entry points is shown in red and blue, respectively. Dash lines show the status of acquired genes in different stages of the lifecycle.

Figure 4. Diagram illustrating the dynamics of HGT in plants.

Horizontal lines and arrows show HGT donors and recipients. Information about HGT in the ancestor of red algae and green plants is based on.