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

Li FW, Melkonian M, Rothfels CJ, Villarreal JC, Stevenson DW, Graham SW, Wong GK, Pryer KM, Mathews S - Nat Commun (2015)

Bottom Line: 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.Our results reveal novel phytochrome clades and establish the basis for understanding phytochrome functional evolution in land plants and their algal relatives.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA.

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.

No MeSH data available.


Related in: MedlinePlus

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 cryptophytes32. †Full-length phytochrome was not available from Charales and its domain structure was inferred.
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f2: 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 cryptophytes32. †Full-length phytochrome was not available from Charales and its domain structure was inferred.

Mentions: The phylogenetic position of cryptophytes remains controversial. They were once thought to be related to stramenopiles and haptophytes (belonging to the kingdom Chromalveolata), but some recent phylogenomic studies place them either as nested within, or sister to, Archaeplastida262728. In our analyses, cryptophyte+Viridiplantae phytochromes form a clade that is sister to glaucophyte phytochromes (Fig. 1 and Supplementary Fig. 2). Also, phytochromes from Viridiplantae and from some cryptophytes share the characteristic PAS–PAS repeat in the C terminus (Fig. 2). These cryptophyte phytochromes differ from the canonical phytochromes in their retention of the conserved histidine phosphorylation site in the kinase domain (Figs 1 and 2). Some cryptophyte phytochromes do not have the PAS–PAS repeat in the C terminus, but instead possess a single PAS followed by a serine/threonine kinase domain (‘PKC' in Figs 1 and 2). Despite this variation in the C terminus, the N-terminal photosensory modules of all cryptophyte phytochromes are monophyletic (Fig. 1 and Supplementary Fig. 2).


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

Li FW, Melkonian M, Rothfels CJ, Villarreal JC, Stevenson DW, Graham SW, Wong GK, Pryer KM, Mathews S - Nat Commun (2015)

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 cryptophytes32. †Full-length phytochrome was not available from Charales and its domain structure was inferred.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525182&req=5

f2: 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 cryptophytes32. †Full-length phytochrome was not available from Charales and its domain structure was inferred.
Mentions: The phylogenetic position of cryptophytes remains controversial. They were once thought to be related to stramenopiles and haptophytes (belonging to the kingdom Chromalveolata), but some recent phylogenomic studies place them either as nested within, or sister to, Archaeplastida262728. In our analyses, cryptophyte+Viridiplantae phytochromes form a clade that is sister to glaucophyte phytochromes (Fig. 1 and Supplementary Fig. 2). Also, phytochromes from Viridiplantae and from some cryptophytes share the characteristic PAS–PAS repeat in the C terminus (Fig. 2). These cryptophyte phytochromes differ from the canonical phytochromes in their retention of the conserved histidine phosphorylation site in the kinase domain (Figs 1 and 2). Some cryptophyte phytochromes do not have the PAS–PAS repeat in the C terminus, but instead possess a single PAS followed by a serine/threonine kinase domain (‘PKC' in Figs 1 and 2). Despite this variation in the C terminus, the N-terminal photosensory modules of all cryptophyte phytochromes are monophyletic (Fig. 1 and Supplementary Fig. 2).

Bottom Line: 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.Our results reveal novel phytochrome clades and establish the basis for understanding phytochrome functional evolution in land plants and their algal relatives.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA.

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.

No MeSH data available.


Related in: MedlinePlus