On plant defense signaling networks and early land plant evolution

Abstract

All land plants must cope with phytopathogens. Algae face pathogens, too, and it is reasonable to assume that some of the strategies for dealing with pathogens evolved prior to the origin of embryophytes - plant terrestrialization simply changed the nature of the plant-pathogen interactions. Here we highlight that many potential components of the angiosperm defense toolkit are i) found in streptophyte algae and non-flowering embryophytes and ii) might be used in non-flowering plant defense as inferred from published experimental data. Nonetheless, the common signaling networks governing these defense responses appear to have become more intricate during embryophyte evolution. This includes the evolution of the antagonistic signaling pathways of jasmonic and salicylic acid, multiple independent expansions of resistance genes, and the evolution of resistance gene-regulating microRNAs. Future comparative studies will illuminate which modules of the streptophyte defense signaling network constitute the core and which constitute lineage- and/or environment-specific (peripheral) signaling circuits.

Keywords: Plant evolution; charophytes; molecular plant–microbe interaction; phytopathology; plant defense; streptophyte algae.

Figure 1.

Key phytopathogen interaction factors across the trajectory of streptophyte evolution. Schematic cladogram (white lines) of the Chloroplastida depicts the deep split of the green lineage into Chlorophyta and Streptophyta about 900 million years ago (divergence times based on Morris et al. [45]). The Streptophyta encompass the paraphyletic streptophyte algae and the monophyletic land plants (Embryophyta). Land plants are likely >500 million years old and consist of the non-vascular bryophytes and the ~430 million year old clade of vascular plants, encompassing lycophytes and euphyllophytes. The euphyllophytes are the clade of ferns, gymnosperms and angiosperms (the latter two are the seed plants). Boxes highlight when – along this trajectory – signaling factors in plant defense are thought to have evolved; brackets further specify the type of data and/or functional significance of a given factor. The asterisks indicate nodes for which data are limited. JA, jasmonic acid; JA-Ile, jasmonic acid-isoleucine; SA, salicylic acid; ET, ethylene; NBS-LRR, nucleotide binding site-leucine-rich repeat; TIR-NBS-LRR, Toll-interleukin 1 receptor-nucleotide binding site-leucine-rich repeat; CC-NBS-LRR, coiled coil-nucleotide binding site-leucine-rich repeat; FLS2, FLAGELLIN SENSITIVE2.