Small One-Helix Proteins Are Essential for Photosynthesis in Arabidopsis

Abstract

The extended superfamily of chlorophyll a/b binding proteins comprises the Light-Harvesting Complex Proteins (LHCs), the Early Light-Induced Proteins (ELIPs) and the Photosystem II Subunit S (PSBS). The proteins of the ELIP family were proposed to function in photoprotection or assembly of thylakoid pigment-protein complexes and are further divided into subgroups with one to three transmembrane helices. Two small One-Helix Proteins (OHPs) are expressed constitutively in green plant tissues and their levels increase in response to light stress. In this study, we show that OHP1 and OHP2 are highly conserved in photosynthetic eukaryotes, but have probably evolved independently and have distinct functions in Arabidopsis. Mutations in OHP1 or OHP2 caused severe growth deficits, reduced pigmentation and disturbed thylakoid architecture. Surprisingly, the expression of OHP2 was severely reduced in ohp1 T-DNA insertion mutants and vice versa. In both ohp1 and ohp2 mutants, the levels of numerous photosystem components were strongly reduced and photosynthetic electron transport was almost undetectable. Accordingly, ohp1 and ohp2 mutants were dependent on external organic carbon sources for growth and did not produce seeds. Interestingly, the induction of ELIP1 expression and Cu/Zn superoxide dismutase activity in low light conditions indicated that ohp1 mutants constantly suffer from photo-oxidative stress. Based on these data, we propose that OHP1 and OHP2 play an essential role in the assembly or stabilization of photosynthetic pigment-protein complexes, especially photosystem reaction centers, in the thylakoid membrane.

Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non‐model organism aided by transcriptomic data integration

“…SEP2 was accumulated to a remarkable extent in both steps of light increase, whereas OHP2 only accumulated in HL plants (Figure ). The accumulation of OHP2 in HL plants confirms its essential role in the assembly and maintenance of both PSs in response to light stress (Beck et al ., ). Even if the physiological function(s) of SEP2 is not yet well understood (Heddad and Adamska, ), its accumulation at increasing growth irradiances indicates its high sensitivity to light stress.…”

A theophylline-responsive riboswitch regulates expression of nuclear-encoded genes in Arabidopsis

“…Failure to assemble or stabilize photosystems causes seedling lethality in ohp1 mutants, which complicates the analysis of the precise gene function. A construct containing the OHP1 cDNA with an aTheoAz in the 3’UTR under control of the CaMV 35S promoter had been used previously to complement the seedling-lethal phenotype of ohp1-1 mutants (Beck et al, 2017). However, treatment of these plants with theophylline did not cause phenotypical changes, presumably because the residual transcript level still allowed the synthesis of sufficient amounts of OHP1 protein.…”

“…Here we show that the aTheoAz incorporated into the 3’-UTR of a GFP expression cassette constitutes an effective riboswitch enabling dose- and time-dependent down-regulation of GFP transcript and protein levels in Arabidopsis. We demonstrate that aptazyme-mediated downregulation of gene expression can be used for physiological studies by conditional complementation of mutants lacking the thylakoid-integral One Helix Protein 1 (OHP1), which is required for synthesis or maintenance of functional photosystems (Beck et al, 2017; Hey and Grimm, 2018; Myouga et al, 2018). The seedling-lethal phenotype of ohp1-1 mutants was overcome by a switchable transgenic copy of the OHP1 gene and treatment of seedlings with theophylline reduced the OHP1 transcript level to near the detection limit.…”

A Light Harvesting Complex-Like Protein in Maintenance of Photosynthetic Components in Chlamydomonas

“…These proteins could be structurally attributed to four subfamilies (OHPs, SEPs, ELIPs, and PsbS) based on the number of transmembrane domains (Heddad and Adamska, 2002;Komenda and Sobotka, 2016). Functional characterization using genetic and biochemical means has revealed distinct role(s) for individual proteins within or among these different subfamilies (Niyogi and Truong, 2013;Dinc et al, 2016;Beck et al, 2017). Msf1 resembles structurally LHClike proteins containing three transmembrane domains (Fig.…”

“…These proteins contain up to four transmembrane domains with conserved chlorophyll-binding sites and have been identified in land plants and green algae (Teramoto et al, 2004(Teramoto et al, , 2006Beck et al, 2017) as well as in cyanobacteria (Kufryk et al, 2008;Cheregi et al, 2012;Staleva et al, 2015;Komenda and Sobotka, 2016). They include the onehelix proteins (OHPs), also named HLIPs (high-lightinduced proteins), two-helix stress-enhanced proteins (SEPs), three-helix early light-induced proteins (ELIPs; for review, see Heddad and Adamska, 2002;Komenda and Sobotka, 2016), and the four-helix PsbS protein that is unable to bind pigments (Kim et al, 1992).…”