Three PsbQ-Like Proteins are Required for the Function of the Chloroplast NAD(P)H Dehydrogenase Complex in Arabidopsis

Abstract

Arabidopsis has three PsbQ-like (PQL) proteins in addition to the PsbQ subunit of the oxygen-evolving complex of PSII. Recent bioinformatic and proteomic studies suggested that the two PQL proteins, PQL1 (At1g14150) and PQL2 (At3g01440), might function in the chloroplast NAD(P)H dehydrogenase (NDH) complex; however, their molecular function has not been characterized. In this study, we examined the function of the chloroplast NDH in the Arabidopsis pql1 and pql2 mutants. Post-illumination increases in Chl fluorescence, which are caused by an NDH-dependent cyclic electron flow, were absent in both mutants, indicating that PQL1 and PQL2 are required for NDH activity. In the thylakoid membranes of wild-type plants, PQL1 and PQL2 were tightly associated with the NDH-PSI supercomplex and protected from protease treatments, while unassembled PQLs were not stably accumulated in mutants lacking known NDH subunits. Subunit stability of the NDH complex was affected differently in the thylakoid membranes of the pql1 and pql2 mutants. These data indicate that PQL1 and PQL2 are novel NDH subunits and differ in their functional roles and in their binding sites in the NDH complex. Furthermore, functional analysis on PQL3 (At2g01918) using the pql3 mutant suggests that PQL3 is also required for NDH activity. Proteins homologous to each PQL protein are found in various plant species, but not in cyanobacteria, algae, mosses or ferns. These results suggest that seed plants that have NDH activity in chloroplasts specifically developed three PQL proteins for the function of the chloroplast NDH complex.

Supercomplex Formation with Photosystem I Is Required for the Stabilization of the Chloroplast NADH Dehydrogenase-Like Complex in Arabidopsis

“…1C). So far, a total of 25 NDH subunits have been identified by various approaches (Rumeau et al, 2005;Ishihara et al, 2007;Ishikawa et al, 2008;Majeran et al, 2008;Shimizu et al, 2008;Peng et al, 2009;Sirpiö et al, 2009aSirpiö et al, , 2009bTakabayashi et al, 2009;Suorsa et al, 2010;Yabuta et al, 2010). If we assume that only one copy of each subunit is included in the complex, the calculated molecular mass of NDH is approximately 690 kD, which is almost identical to that of the NDH complex detected in lhca5 lhca6.…”

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b6/f Supercomplex

“…More recent studies have also confirmed that PPL2 (17 kD) is a novel subunit associated with the NDH complex in Arabidopsis (Peng et al, 2009;Suorsa et al, 2009). In addition, several PsbQ-like (PQL) proteins (including PsbQ-F1 and PsbQ-F2, both 17 kD) have been shown to be necessary for the function of the NDH complex in Arabidopsis (Majeran et al, 2008;Peng et al, 2009;Suorsa et al, 2009;Yabuta et al, 2010). Furthermore, PQL1 and PQL2 were found to be tightly associated with the NDH-PSI supercomplex (Suorsa et al, 2010;Yabuta et al, 2010).…”

Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO2 in the Bundle Sheath Cell of Zea mays

“…Studies with Arabidopsis and tobacco have shown that failure to form an active chloroplast NDH complex results in a characteristic change in the kinetics of Chl fluorescence in response to darkening , Rumeau et al, 2005, Munshi et al, 2006, Ishihara et al, 2007, Ishikawa et al2008, Peng et al, 2009, Takabayashi et al, 2009, Suorsa et al, 2010, Yabuta et al, 2010. Figure 2 compares this light-dark transient for the maize mutants ZmNdho and ZmNdhn and respective normal sibling controls.…”

“…At least 11 plastid and 25 nuclear genes encode NDH subunits and related protein factors in Arabidopsis (Ifuku et al, 2011. Serial disruption of several nuclear genes encoding structural subunits or assembly factors resulted in failed NDH supercomplex assembly and disrupted electron flow to PQ (plastoquinone) in the dark (Rumeau et al, 2005, Munshi et al, 2006, Ishihara et al, 2007, Ishikawa et al, 2008, Takabayashi et al, 2009, Peng et al, 2010, Suorsa et al, 2010, Yabuta et al, 2010, Armbruster et al, 2013. Chloroplastic NDH has been assigned to a redundant NAD(P)H-dependent PSI cyclic electron transport pathway in C 3 plants (Nixon 2000).…”