Protoplasma

, Volume 254, Issue 1, pp 603–607 | Cite as

Cyanobacterial origin of plant phytochromes

Short Communication

Abstract

Phytochromes are widely distributed photoreceptors with similar domain arrangements. The evolutionary origin of plant and green algal phytochromes is currently under debate. We used different algorithms to generate multiple phylogenetic trees for the N-terminal chromophore module and the C-terminal histidine kinase domains. The evolution of the chromophore module and the histidine kinase (like) regions follows different patterns, indicating several rearrangements between both parts of the protein. Out of 22 trees, 19 revealed a close relationship between cyanobacteria and Archaeplastida, the group encompassing plants and green algae. Opposed to other studies, a cyanobacterial origin of plant phytochromes is strongly supported by our results.

Keywords

Maximum likelihood Bayesian inference Photosensitive core module Histidine kinase 

Plants respond to light in manifold ways, and the best studied photoreceptors that control developmental processes are the phytochromes. These biliproteins have been discovered by their red/far-red photoreversible behavior (Butler et al. 1959; Hershey et al. 1984). Typical phytochrome responses are switched on by a red light pulse and switched off by subsequent far-red, due to the photoconversion between the inactive “Pr” and the active “Pfr” form (Schäfer and Nagy 2006). When the first phytochromes and phytochrome-like proteins were found in cyanobacteria (Kehoe and Grossman 1996; Lamparter et al. 1997; Yeh et al. 1997), it seemed clear that plant phytochromes were inherited from cyanobacteria via the endosymbiosis pathway; other bacterial phytochromes were initially not known. In the meantime, many phytochrome sequences have been found in cyanobacteria, other bacteria, and fungi (Lamparter 2004; Mandalari et al. 2013). Phylogenetic studies that were performed under inclusion of plant, cyanobacterial and other bacterial and fungal sequences yielded different results with respect to the origin of plant phytochromes. In our own studies, a link between cyanobacteria and plant phytochromes was missing which led us to assume that plant phytochromes have originated from a species outside cyanobacteria (Lamparter 2004). Such a distant relationship was also found by other groups (Karniol et al. 2005); later studies provided evidence for a closer relationship between cyanobacteria and plants (Rottwinkel et al. 2010; Ulijasz et al. 2008). It seemed therefore difficult to decide whether plant phytochromes are of cyanobacterial origin or whether they have originated from other prokaryotes. In order to clarify this question, we have recently performed a comprehensive study that was based on a large number of sequences by the use of different alignment programs, different tree construction programs, and various parameters (Buchberger and Lamparter 2015). The studies were performed separately for the N-terminal photosensory core module (PCM, consisting of PAS-GAF and PHY domains) and the C-terminal histidine (His) kinase. Seventeen PCM trees and 13 His kinase trees were compared. Plant and Zygnematales phytochromes, which together belong to the group of Streptophytes, formed one group. A cyanobacterial origin of plant phytochromes was the most conclusive evolutionary pathway in this study. In another study, evidence was provided for a non-cyanobacterial origin of plant phytochromes. This work included novel phytochrome sequences from Cryptophytes, Prasinophytes, and Glaucophytes (Duanmu et al. 2014) that were not included in previous analyses. When the authors constructed phylogenetic trees without these sequences, the Streptophyte phytochromes appeared as a sister group of cyanobacterial phytochromes. The insertion points of the novel sequences were at the base of the Streptophyte branch, indicating a common origin of all these phytochromes. The entire group with the exception of Cryptophytes is a member of the Archaeplastida. Cryptophytes arose from secondary endosymbiosis and have genes of green algal and red algal origin (Curtis et al. 2012), which justifies the assumption of a common origin of Archaeplastida and Cryptophyte PCMs. In Duanmu et al. (2014), the Archaeplastida branch now originated at a position separate from cyanobacteria. A study which encompasses mainly phytochromes of eukaryotic origin also came to the conclusion of non-cyanobacterial origin of plant phytochromes (Li et al. 2015).

In order to resolve the contradiction regarding the origin of plant phytochromes, we performed phylogenetic studies with different programs using phytochrome sequence datasets with or without the inclusion of Glaucophytes, Prasinophytes, and Cryptophytes. Out of the 446 phytochrome sequences used in our previous study (Buchberger and Lamparter 2015), we selected 60 sequences as a basis for the present study. We reduced fungi and diatoms to one sequence per group, Streptophytes (land plants and Caraphyceen algae) to 14 and cyanobacteria to 12 sequences. The other 32 sequences belong to α-, β-, δ-, and γ-proteobacteria; flavobacteria; or other bacterial groups. In this way, all relevant clades of the previous study are represented. In addition, we selected five phytochrome sequences from Prasinophytes, one from the Cryptophyte Guillardia theta and two from the Glaucophyte Cyanophora paradoxa from the NCBI database. Datasets with and without these sequences were subjected to the same alignment and phylogeny programs in order to find out whether this addition leads to a separation of plant and cyanobacterial clades as described by (Duanmu et al. 2014). Each protein sequence was split into PCM and His kinase regions, and phylogenetic analyses were performed separately. The selected G. theta sequence is incomplete and lacks information about the C-terminal part, and one of the two C. paradoxa sequences has no His Kinase in its C-terminus. In those two cases, only the PCM region was used. Altogether, four datasets were generated: PCM sequences with and without Prasinophytes/Cryptophytes/Glaucophytes and His kinase sequences with and without Prasinophytes/Glaucophytes. Following alignments with MUSCLE, phylogenetic trees were constructed using neighbor joining (NJ), Fitch, parsimony, and maximum likelihood (ML) from the Phylip 3.69 program package (JTT matrix); ML, NJ, and minimum evolution from Mega 6 (WAG, JTT, and JTT matrix, respectively); PhyML 3.1 (with three different matrices); and MrBayes 3.24 (WAG model and approximately 5,000,000 generations until the deviation of split frequencies fell below 0.5). All studies performed with the Mega package were combined with bootstrapping. Three of the four trees that were generated with MrBayes are shown with collapsed clades in Figs. 1a, b and 2.
Fig. 1

Phylogenetic trees generated with MrBayes presented with collapsed clades. Above: Tree including 60 PCM sequences. Below: Tree with additional 8 Prasinophyte, Glaucophyte, or Cryptophyte sequences

Fig. 2

Phylogenetic tree generated with MrBayes based on 66 phytochrome His kinase sequences

In the PCM trees, the new sequences from Glaucophytes, Cryptophytes, and Prasinophytes were most often found at the base of the Archaeplastida branch; in few cases, single members were placed outside this branch. The positions of cyanobacteria and Archaeplastida varied between four patterns termed A, B, C, or D (Table 1). In pattern A, Archaeplastida and cyanobacteria appear as sister groups. In pattern B, a similar relationship is obtained but few sequences are placed among or between both groups. In pattern C, Archaeplastida are located at the base of the tree, quite distinct from cyanobacteria. In pattern D, both Archaeplastida and cyanobacteria are located at the base of the tree. All trees that follow pattern D could be changed to pattern A by manually setting an appropriate root. We therefore regard both patterns A and D as support for the close relationship between Archaeplastida and cyanobacteria.
Table 1

Result of phylogenetic trees constructed with different programs

 

PCMa

PCM + 8b

Mega NJ

A

D→A

Phylip NJ

A

A

Fitch

A

A

Mega ME

A

D→A

Phylip Protpars

C

A

Mega ML

A

D→A

Phylip ProML

B

B

PhyML JTT

D→A

D→A

PhyML LG

D→A

D→A

PhyML WAG

D→A

D→A

MrBayes

A

A

A = Archaeplastida and cyanobacteria PCMs are sister groups (in one case with one other bacterium within the Archaeplastida group); B = as A, but two to four other PCM grouped together with Archaeplastida or cyanobacteria (sometimes Glaucophytes separate from Archaeplastida branch); C = Archaeplastida PCM is at the base of the tree, next to Acariochloris and four other bacteria; D = Archaeplastida PCM is at the base of the tree, and cyanobacteria are at the base of the remaining species; D→A = pattern D can be converted to pattern A by rerooting the tree

aBased on 60 PCM sequences

bBased on 68 sequences with the inclusion of Prasinophyte, Cryptophyte, and Glaucophyte phytochromes

Pattern A was obtained in 6 of the 11 PCM trees that were constructed without Glaucophytes, Prasinophytes, or Cryptophytes, and in 3 trees, pattern D was obtained (Table 1). When the trees were constructed with the inclusion of these sequences, patterns A and D were obtained four and six times, respectively (Table 1). Bootstrap values at the branch points of Archaeplastida and cyanobacteria were in the range of 0.3–0.4, and posterior probabilities of MrBayes were 0.6. The majority of all PCM trees are thus consistent with a cyanobacterial origin of Archaeplastidal PCM.

The present analysis has thus strengthened the idea of an endosymbiotic evolutionary origin of plant phytochromes. Cyanobacterial and plant phytochromes have the same chromophore binding site, which differs from that of other bacteria and fungi (Lamparter 2004). In plants, chromophore synthesis is located in the plastid (Muramoto et al. 2005). Moreover, cyanobacteria and plants have a bilin chromophore with reduced ring A and other groups incorporate a biliverdin chromophore with a double bond in ring A. Therefore, the results of our phylogenetic analysis fit well with other phytochrome-related features that plants and cyanobacteria have in common.

Opposed to the studies of Duanmu et al. (2014), the relationship between phytochromes of Archaeplastida and cyanobacteria is confirmed here even with the inclusion of Prasinophyte, Cryptophyte, and Glaucophyte sequences. We therefore consider the cyanobacterial origin of Archaeplastida as the most likely scenario. A misalignment of sequences, induced by the Prasinophyte, Cryptophyte, and Glaucophyte sequences, could be the reason for their results. The phylogenetic study by Li et al. (2015) was performed on the basis of all phytochrome domains including the His kinase. According to our studies, the N- and C-terminal fractions of phytochromes have a different evolution.

In the His kinase trees, Glaucophyte, Prasinophyte, and Cryptophyte sequences are also most often found at the base of the Archaeplastida branch. Thalassiosira pseudonana, the representative of diatoms, is often found as a sister of Archaeplastida. In some cases, the fungal representative Ustilago maydis is close to Archaeplastida, and a close relationship between fungal and diatom sequences is also often found. In line with our previous study, cyanobacterial His kinase sequences are found in different branches, here in two branches comprising two or more members. One subgroup of the cyanobacteria appears often closely related to the eukaryote branch, but another bacterial sequence from the α-proteobacterium Magnetospirillum gryphiswaldense is always among those sequences as the closest relative of the eukaryotic ones. A cyanobacterial origin of eukaryotic His kinase sequences is thus not supported, leading to the conclusion that a rearrangement between N- and C-terminal moieties occurred in the early evolution of Archaeplastida as discussed before (Buchberger and Lamparter 2015). Because some Prasinophyte phytochromes (e.g., from Nephroselmis pyriformis) have a domain arrangement similar to the Streptophytes with two PAS domains between PCM and His kinase, a rearrangement that formed this particular domain order has most likely occurred as a single event during the early evolution of Archaeplastida. In the Streptophyte lineage, phytochromes with other domain arrangements were apparently lost. Fungal, Glaucophyte, and Prasinophyte phytochromes can have a C-terminal response regulator. In view of the different origins of the PCM, it is impossible that these phytochromes are derived from a common ancestor. Their common domain pattern, which is nevertheless different from that of bacterial phytochromes, arose, therefore also from rearrangements between N- and C-terminal moieties.

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Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Karlsruhe Institute of Technology (KIT)Botanical InstituteKarlsruheGermany

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