COMMENTARY Algae hold clues to eukaryotic origins of plant phytochromes Sarah Mathews1 Centre for Australian National Biodiversity Research, National Research Collections Australia, theory, which holds that plant phytochromes CSIRO National Facilities and Collections, Canberra ACT 2601, Australia were acquired by gene transfer from the cya- nobacterial endosymbiont (EGT) that gave rise to chloroplasts. Plants use phytochrome photoreceptors to deeply. The ability of phytochrome to mea- Until relatively recently, phytochromes determine their proximity to other plants, sure the R:FR ratio arises from its photo- were unknown outside of land plants, except to gauge the intensity of vegetational shade, reversibility. It interconverts between two in closely related streptophyte algae. This and to determine whether they are near the forms, a red absorbing form (Pr) and a far- changed with the discovery of phytochrome- surface of bare soil or buried under leaf red absorbing form (Pfr), which occur in like proteins in cyanobacteria (4, 5), and litter. In each case, phytochromes are mea- a dynamic equilibrium determined by the thereafter, with the discovery of a vast diver- suring the ratio of red (R) to far-red (FR) R:FR ratio in ambient light. Although phy- sity of phytochrome-related proteins in light in the environment, and plants are tochromes have diversified independently in bacteria, fungi, diatoms, and brown algae. using the information to elicit critical de- mosses, ferns, and seed plants (2), the differ- Amongthesearephytochromestunedto velopmental responses, such as delaying the ent members of the phytochrome family in yellow, green, blue, and violet wavelengths, germination of seeds under a leaf litter or these lineages and across plants have very as well as to R and FR, and in some, the growing taller and reproducing earlier when similar absorption maxima, centered on bilin chromophore confers redox instead of neighbors impinge on their access to light 660 nm for Pr and 730 nm for Pfr. For plants light sensing abilities (6). Early phylogenetic (1). In open environments, the R:FR ratio is in terrestrial environments, the importance of analyses to understand diversity in this near 1; under a dense canopy or under leaf the R:FR ratio is universal, and the spectral larger phytochrome superfamily were in- litter, it may fall to as low as 0.2, due to properties of phytochromes appear to have conclusive regarding relationships among absorption of most of the light available for changed little through the ∼500 million years plant and bacterial phytochromes, but they photosynthesis (400–700 nm) by plant pig- of land plant evolution. The origins of phy- suggested that cyanobacterial phytochromes ments. Similarly, in soils, short wavelengths tochrome, however, have remained mysteri- were more closely related to bacterial than are scattered in the first few millimeters, ous. In PNAS, Duanmu et al. (3) provide to plant phytochromes (7, 8). In one study, whereas longer wavelengths penetrate more evidence that contradicts the prevailing the N-terminal photosensory core and the C-terminal regulatory region were analyzed separately, providing strong evidence that C Viridiplantae Viridiplantae termini of plant and cyanobacterial phyto- A B chromes were not closely related (9). To- Rhodophyta Cryptophyta gether, the results of these studies contradicted Glaucophyta Glaucophyta EGT. Herdman et al. (10) also failed to resolve Cryptophyta relationships among cyanobacterial, bacterial, Bacteria and plant phytochromes, but nonetheless ar- Alveolates Bacteria, Cyanobacteria gued that similarity among the three types resulted from EGT. Vierstra and Davis (11) Stramenopiles Bacteria argued for EGT based on examination of se- Rhizaria Stramenopiles, Viruses quence alignments and the organization of Haptophyta Unikonts domains,andEGThasremainedthefavored hypothesis. Excavates A major obstacle to resolving the question Unikonts of plant phytochrome origins has been the lack of phytochrome data from a greater Fig. 1. (A) Simplified unrooted tree of eukaryotes [after Burki et al. (16)] showing the major lineages: Viridplantae (green diversity of eukaryotes, especially from eu- algae and land plants), rhodophytes (red algae), glaucophytes (microalgae with Cyanobacteria-like plastids), Crypotphytes karyotes in the Archaeplastida, Viridiplantae and Haptophytes (unicellular algae, some that retain plastids obtained via secondary endosymbiosis), Alveolates (dino- flagellates, ciliates, and ampicomplexan parasites), Stramenopiles (water molds, diatoms, brown and golden algae), (green plants and algae), Rhodophyta (red Rhizaria (including amoebaflagellates and radiolarians), Excavates (free-living parasitic and unicellular forms, including algae), and Glaucophyta (microalgae with parasties such as Euglena, Trypanosoma,andGiardia), and Unikonts (including animals and fungi). (B) Simplified Cyanobacteria-like choroplasts) (relationships unrooted tree of phytochromes in prokaryotes and eukaryotes (3). In stramenopiles, phytochromes are found in diatoms and brown algae. In unikonts, phytochromes are found in fungi. The diverse bacterial lineage that is sister to unikonts and stramenopiles includes photosynthetic, nitrogen-fixing, and plant pathogenic bacteria bacteria, including Author contributions: S.M. wrote the paper. the common vector for genetic transformation of Arabidopsis thaliana, Agrobacterium tumefaciens. Cyanobac- The author declares no conflict of interest. teria are sister to another, similarly diverse clade of photosynthetic and heterotrophic bacteria that includes the extremophile Dienococcus radiodurans and methylotrophic species of Methylobacterium. The remaining, un- See companion article on page 15827. placed bacterial lineage is exclusively photosynthetic. 1Email: [email protected].

15608–15609 | PNAS | November 4, 2014 | vol. 111 | no. 44 www.pnas.org/cgi/doi/10.1073/pnas.1417990111 Downloaded by guest on September 25, 2021 among eukaryotes are summarized in Fig. scenario. It is the only phytochrome thus far prasinophyte algae allowed them to es- COMMENTARY 1A). Duanmu et al. address this by se- detected that shares with Viridiplantae tablish that diverse members of the chlo- quencing and assembling transcriptomes phytochromes a double internal PAS (Per- rophyte algae do possess phytochromes, from a glaucophyte and several prasinophyte ARNT-Sim) repeat that separates the PCM despite their absence in sequenced genomes algae and by including phytochrome se- from the C-terminal histidine-kinase-related of species from Chlamydomonas, Chlorella, quences from these assemblies in a matrix module (HKM). Glaucophytes have a single Volvox, Bathycoccus, and Ostreococcus.More- with a good representation of published internal PAS (14), whereas prokaryotic over, they establish that phytochromes of eukaryotic and prokaryotic phytochromes. phytochromes lack an internal PAS (6). prasinophytes share light-mediated signaling Two important phylogenetic results emerge The phylogenetic analysis of the HKM by mechanisms with those of land plants, in- from their analyses of the three domains of cluding strong diurnal regulation of gene the N-terminal photosensory core module Duanmu et al. expression preceded by redistribution of (PCM). First, there is clear evidence for demonstrate that the phytochrome from the cytoplasm to the two independent origins of eukaryotic strategic choice of a nucleus. Unlike plant phytochromes, how- PCM; sequences from diatoms and brown ever, prasinophyte phytchromes are tuned algae (stramenopiles) and fungi form one relatively small number to wavelengths that travel farther through lineage nested within bacteriophytochromes, of study organisms can seawater than do R and FR, and their HKM whereas sequences from Archaeplastida and retain histidine kinase catalytic activity. the cryptophyte, Guillardia theta,form greatly advance our As significant players in carbon cy- another monophyletic lineage (Fig. 1B). The understanding of cling, prasinophytes are ecologically im- distinctness of the two eukaryotic phyto- phylogeny and function. chrome lineages is also reflected in the portant in their own right. Phylogenetically, domain structures of their C-terminal re- Duanmu et al. was less conclusive. The results they also occupy a key position. They split gions. Second, cyanobacterial PCM are nested do not provide statistically strong support for earlier from the chlorophyte branch of within prokaryotic PCM and are more closely a close relationship between green plant and Viridiplantae than do the model organ- related to bacterial, fungal, and stramenopile cyanobacterial HKM, but they do suggest isms such as Chlamydomonas reinhardtii, PCM than they are to archaeplastid PCM. that the history of glaucophyte HKM differs Chlorella vulgaris, and Volvox carteri (12), This suggests that the heterotrophic ancestor from that of cryptophytes and Viridiplantae. and they retain certain features of land plants of Archaeplastida may have possessed a phy- Puzzles clearly remain to be addressed in not retained by the model species (15). tochrome before the primary endosymbiotic this regard. Altogether, the results of Duanmu et al. event, or that EGT from the cyanobacterial Within Viridiplantae, however, the demonstrate that the strategic choice of a endosymbiont occurred very early, before the findings of Duanmu et al. fill important relatively small number of study organisms divergence of Viridplantae, Rhodophyta, and gaps in our knowledge of phytochrome can greatly advance our understanding of Glaucophyta from one another. The pho- evolution and function. Their focus on phylogeny and function. tosensory core of plant phytochromes thus has been evolving independently from that of cyanobacterial phytochromes for up to 1 Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light- 9 Lamparter T (2004) Evolution of cyanobacterial and plant 1,200 million years, based on fossil records regulated plant growth and development. Curr Top Dev Biol phytochromes. FEBS Lett 573(1-3):1–5. 91:29–66. 10 Herdman M, Coursin T, Rippka R, Houmard J, Tandeau de for green algae (12). 2 Mathews S (2006) Phytochrome-mediated development in land Marsac N (2000) A new appraisal of the prokaryotic origin of Notably, phytochromes have not been plants: Red light sensing evolves to meet the challenges of changing eukaryotic phytochromes. J Mol Evol 51(3):205–213. Mol Ecol – detected in red algal genomes, and in this light environments. 15(12):3483 3503. 11 Vierstra RD, Davis SJ (2000) Bacteriophytochromes: New tools 3 Duanmu D, et al. (2014) Marine algae and land plants share for understanding phytochrome signal transduction. Semin Cell Dev Proc Natl Acad Sci USA context, the position of the cryptophyte conserved phytochrome signaling systems. Biol 11(6):511–521. – Guillardia theta in the PCM trees (Fig. 1B)is 111:15827 15832. 12 Leliaert F, et al. (2012) Phylogeny and molecular evolution of 4 Kehoe DM, Grossman AR (1996) Similarity of a chromatic the green algae. Crit Rev Plant Sci 31:1–46. interesting. Cryptophytes are among the sev- adaptation sensor to phytochrome and ethylene receptors. Science 13 Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. 273(5280):1409–1412. eral organisms that obtained plastids from Annu Rev Plant Biol 59(1):491–517. 5 Hughes J, et al. (1997) A prokaryotic phytochrome. Nature red algae via a secondary endosymbiosis event 14 Rockwell NC, et al. (2014) Eukaryotic algal phytochromes 386(6626):663. span the visible spectrum. Proc Natl Acad Sci USA 111(10): (13). Rhodophytes are sister to Viridiplantae 6 Auldridge ME, Forest KT (2011) Bacterial phytochromes: – in the organismal tree, and this is the position More than meets the light. Crit Rev Biochem Mol Biol 46(1): 3871 3876. 67–88. 15 Worden AZ, et al. (2009) Green evolution and dynamic of G. theta in the PCM tree of Duanmu et al., 7 Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: adaptations revealed by genomes of the marine Micromonas Science – suggesting that phytochromes were present Sensors of bilins and light. Trends Plant Sci 7(8):357–366. picoeukaryotes . 324(5924):268 272. in red algae before the secondary endosym- 8 Karniol B, Wagner JR, Walker JM, Vierstra RD (2005) 16 Burki F, Okamoto N, Pombert JF, Keeling PJ (2012) The Phylogenetic analysis of the phytochrome superfamily reveals evolutionary history of haptophytes and cryptophytes: phylogenomic biosis event. The structure of one of the distinct microbial subfamilies of photoreceptors. Biochem J evidence for separate origins. Proc R Soc B-Biol Sci 279(1736): G. theta phytochromes is consistent with this 392(Pt 1):103–116. 2246–2254.

Mathews PNAS | November 4, 2014 | vol. 111 | no. 44 | 15609 Downloaded by guest on September 25, 2021