Phytochrome diversity in green plants and the origin of canonical plant phytochromes

Abstract

Phytochromes are red/far-red photoreceptors that play essential roles in diverse plant morphogenetic and physiological responses to light. Despite their functional significance, phytochrome diversity and evolution across photosynthetic eukaryotes remain poorly understood. Using newly available transcriptomic and genomic data we show that canonical plant phytochromes originated in a common ancestor of streptophytes (charophyte algae and land plants). Phytochromes in charophyte algae are structurally diverse, including canonical and non-canonical forms, whereas in land plants, phytochrome structure is highly conserved. Liverworts, hornworts and Selaginella apparently possess a single phytochrome, whereas independent gene duplications occurred within mosses, lycopods, ferns and seed plants, leading to diverse phytochrome families in these clades. Surprisingly, the phytochrome portions of algal and land plant neochromes, a chimera of phytochrome and phototropin, appear to share a common origin. Our results reveal novel phytochrome clades and establish the basis for understanding phytochrome functional evolution in land plants and their algal relatives.

Figure 1. Phylogeny of phytochromes.

Terminal clades are collapsed into higher taxonomic units (usually orders or classes) for display purposes. Orange circles indicate inferred gene duplications. Italicized capital letters within each circle correspond to duplication events mentioned in the text, and the numbers/letters adjacent to each orange circle are the names of gene duplicates. Canonical plant phytochromes originated in an ancestor of streptophytes (green star), and some charophyte algae retain non-canonical phytochromes (PHYX1 and PHYX2). Phytochrome domain architectures are shown on the right. Domains that are not always present are indicated by dashed outlines. Domain names: GAF (cGMP phosphodiesterase/adenylate cyclase/FhlA); H/KD (histidine phosphorylation site (H) in the histidine kinase domain (KD)); PAS (Per/Arnt/Sim); PHY (Phytochrome); PKC (Protein Kinase C); REC (Response Regulator); and RING (Really Interesting New Gene). *Traditional Archaeplastida do not include cryptophytes.

Figure 2. The diversity and evolution of phytochrome C-terminal output module.

The tree depicts the organismal phylogeny of all the phytochrome-containing lineages. The domain architecture of the C-terminal regulatory module characteristic of each lineage is indicated on the right connected by dashed lines. The N-terminal photosensory module has a largely conserved domain sequence of PAS–GAF–PHY, and is not drawn here. The substitution of the histidine phosphorylation site (H) in the histidine kinase domain (KD) occurred subsequent to the divergence of prasinophytes. The canonical plant phytochrome is restricted to streptophytes (in grey box); Zygnematales and Coleochaetales also have non-canonical plant phytochromes. Domain names: PAS (Per/Arnt/Sim); PKC (Protein Kinase C); REC (Response Regulator); and RING (Really Interesting New Gene). *Traditional Archaeplastida do not include cryptophytes. †Full-length phytochrome was not available from Charales and its domain structure was inferred.

Figure 3. Phylogeny of neochromes and phytochromes.

The support values are shown for the neochrome branches only, in the following order: maximum likelihood bootstrap support (BS) from general time reversible (GTR) nucleotide model/Bayesian posterior probabilities (PP) from GTR nucleotide model/aLRT support from codon model/maximum likelihood bootstrap values from Jones-Taylor-Thornton (JTT) amino acid model/Bayesian posterior probabilities from JTT amino acid model. ‘*' Indicates all the support values=100 or 1.0. ‘−' denotes BS<70, aLRT<70, or PP<0.95. Branches are thickened when BS>70, aLRT>70, and PP>0.95.

Figure 4. Phylogeny of bryophyte phytochromes.

Previously identified phytochromes are in bold font. Support values associated with branches are maximum likelihood bootstrap values (BS)/Bayesian posterior probabilities (PP); these are only displayed (along with thickened branches) if BS>70 and PP>0.95. Thickened branches without numbers are 100/1.0. The position of orange circles indicates inferred gene duplications. Italicized capital letters within each circle correspond to the duplication event mentioned in the text, and the numbers/letters adjacent to each circle indicate the names of the gene duplicates.

Figure 5. Phylogeny of fern and lycophyte phytochromes.

Previously identified phytochromes are shown in bold. Support values associated with branches are maximum likelihood bootstrap values (BS)/Bayesian posterior probabilities (PP); these are only displayed (along with thickened branches) if BS>70 and PP>0.95. Thickened branches without numbers are 100/1.0. The position of orange circles estimates the origin of inferred gene duplications. Italicized capital letters within each circle correspond to the duplication event mentioned in the text, and the numbers/letters adjacent to each circle indicate the names of the gene duplicates.