YCF1: A Green TIC?
Supplementary Material
Abstract
A pivotal step in the transformation of an endosymbiotic cyanobacterium to a plastid some 1.5 billion years ago was the evolution of a protein import apparatus, the TOC/TIC machinery, in the common ancestor of Archaeplastida. Recently, a putative new TIC member was identified in Arabidopsis thaliana: TIC214. This finding is remarkable for a number of reasons: (1) TIC214 is encoded by ycf1, so it would be the first plastid-encoded protein of this apparatus; (2) ycf1 is unique to the green lineage (Chloroplastida) but entirely lacking in glaucophytes (Glaucophyta) and the red lineage (Rhodophyta) of the Archaeplastida; (3) ycf1 has been shown to be one of the few indispensable plastid genes (aside from the ribosomal machinery), yet it is missing in the grasses; and (4) 30 years of previous TOC/TIC research missed it. These observations prompted us to survey the evolution of ycf1. We found that ycf1 is not only lacking in grasses and some parasitic plants, but also for instance in cranberry (Ericaceae). The encoded YCF proteins are highly variable, both in sequence length and in the predicted number of N-terminal transmembrane domains. The evolution of the TOC/TIC machinery in the green lineage experienced specific modifications, but our analysis does not support YCF1 to be a general green TIC. It remains to be explained how the apparent complete loss of YCF1 can be tolerated by some embryophytes and whether what is observed for YCF1 function in a member of the Brassicaceae is also true for, e.g., algal and noncanonical YCF1 homologs.
Some of the best evidence we have for the monophyly of plastids is how they import proteins (McFadden and van Dooren, 2004; Zimorski et al., 2014). Establishing a machinery that translocates proteins across the two membranes separating the organelle’s stroma from the cytosol was crucial for the transition of the endosymbiotic diazotrophic-like cyanobacterium to a plastid in the heterotrophic host (Cavalier-Smith, 2000; McFadden and van Dooren, 2004; Dagan et al., 2013). It was also a prerequisite for the successful transfer of genetic material from the endosymbiont to the host nucleus through endosymbiotic gene transfer (EGT; Martin et al., 1993). Most of the EGT that stripped the plastid genome of its coding capacity occurred in the common ancestor from which the three archaeplastidal lineages—Glaucophyta, Rhodophyta (red lineage), and Chloroplastida (green lineage)—evolved (Martin et al., 1998; Zimorski et al., 2014).
Two main protein complexes mediate plastid protein import: the translocon on the outer envelope of chloroplasts (TOC) and the translocon on the inner envelope of chloroplasts (TIC). In accordance with the majority of EGT events, the main TOC/TIC components evolved in the common ancestor of Archaeplastida (Timmis et al., 2004; Kalanon and McFadden, 2008). Most proteins of the TIC complex are of cyanobacterial origin. However, all previously identified TOC and TIC components are encoded on nuclear DNA (Gould et al., 2008; Kalanon and McFadden, 2008; Shi and Theg, 2013), and, thus far, only TIC40 is unique to the Chloroplastida.
Recently, Kikuchi et al. (2013) found the plastid-encoded YCF1 to be part of a 1-MD membrane protein complex that included TIC20. This complex contained neither TIC40 nor TIC110 components that were previously identified (Kessler and Blobel, 1996; Chou et al., 2003), but three novel ones, including YCF1 (Kikuchi et al., 2013). YCF1 was the first plastid-encoded protein identified whose presence was shown to be essential for the survival of Chlamydomonas reinhardtii and tobacco (Nicotiana tabacum), but whose function remained elusive (Boudreau et al., 1997; Drescher et al., 2000). YCF1—or in accordance with its newly proposed function, TIC214—would represent the first plastid-encoded protein of the TIC complex. It would also add to the set of TIC components (including TIC40 and a full-length TIC62) that is unique to the green lineage. In the course of evolution, organelles have lost or transferred 1000s of genes to the host nucleus, but they hardly ever gained any. That alone is remarkable and the apparent lack of ycf1 in Glaucophytes and Rhodophytes (whose import apparatus evolved from the same ancestral TOC/TIC as that of Chloroplastida) prompted us to inspect the distribution and sequence diversity of ycf1 in more detail.
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This work is supported by a Grant GO1825/4-1 from the Deutsche Forschungsgemeinschaft to S.B.G.
AUTHOR CONTRIBUTIONS
J.d.V. and F.L.S. performed the computational analysis. S.B.G. and J.S. designed the study. All authors discussed the results and commented on the article that J.d.V., B.B., and S.B.G. wrote.