Differential use of two cyclic electron flows around photosystem I for driving CO ₂ -concentration mechanism in C ₄ photosynthesis

Abstract

Whereas linear electron flow (LEF) in photosynthesis produces both ATP and NADPH, the cyclic electron flow (CEF) around photosystem I has been shown to produce only ATP. Two alternative routes have been shown for CEF; NAD(P)H dehydrogenase (NDH)-and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flows, but their physiological relevance has not been elucidated in detail. Meanwhile, because C 4 photosynthesis requires more ATP than does C3 photosynthesis to concentrate CO2, it has not been clear how the extra ATP is produced. In this study, to elucidate whether CEF contributes to the additional ATP needed in C4 photosynthesis, we estimated the amounts of PGR5, which participates in FQR-dependent flow, and NDH-H, a subunit of NDH, in four C 4 species. Although the expression profiles of PGR5 did not correlate well with the additional ATP requirement, NDH was greatly expressed in mesophyll cells in the NAD-malic enzyme (ME) species, and in bundle-sheath cells in NADP-ME species, where there is a strong need for ATP in the respective cells. Our results indicate that CEF via NDH plays a central role in driving the CO2-concentrating mechanism in C4 photosynthesis.ATP synthesis ͉ ferredoxin:plastoquinone oxidoreductase ͉ NAD(P)H dehydrogenase ͉ PGR5 ͉ plant D uring plant photosynthesis, both ATP and NADPH are produced by the linear electron flow (LEF) using both photosystem (PS)I and PSII. Alternatively, ATP can also be produced by cyclic electron flow (CEF) without production of NADPH. Because the ratio of ATP͞NADPH required for CO 2 fixation changes, depending on activities of photorespiration or nitrate assimilation to glutamate, balancing between CEF and LEF is important to perform C 3 photosynthesis effectively (1-4).There are two known pathways of CEF around PSI; chloroplastic NAD(P)H dehydrogenase (NDH)-dependent flow and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flow. NDH complex was identified on the basis of high homology with respiratory complex I in bacteria and mitochondria, when plastid genomes of tobacco (5) and liverwort (6) were completely sequenced. To elucidate the function of NDH complex, several laboratories inactivated the tobacco ndh genes by the plastid transformation technique. Although NDH-inactivated tobacco plants showed normal growth under standard conditions (7-10), environmental stress, such as heat, high light, or decreased air humidity, causes retarded growth, suggesting that the absence of the ATP produced by NDH-dependent CEF makes it more difficult to adapt to changing environmental conditions (9,11,12).On the contrary, the molecular identity of FQR had not been revealed. However, a mutant analysis of Arabidopsis identified the protein PGR5, which is essential for FQR-mediated CEF, although PGR5 itself has no known redox motif (13).Involvement of PGR5 in FQR-mediated CEF is supported by the report that ssr2016 in Synechocystis sp. PCC 6803, homologue of Arabidopsis pgr5, is also required for FQR activity (14). Double mutants defective in both NDH-and FQR-depende...

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

“…S1) without the need for PSI cyclic photophosphorylation (Laisk et al, 2005). This contrasts with Takabayashi et al (2005), who postulated a central role for NDH-dependent cyclic electron flow in the BSC. We point out that the latter model provided no mechanism for balancing the CO 2 fluxes in the MC-BSC system, leading to a concentration of CO 2 in the BSC.…”

“…Maize MC and BSC plastid proteomes revealed expression of 23 NDH-associated components involving eight chloroplast and 26 nuclear gene homologs (Friso et al, 2010). Moreover, elevated expression of NDH in the maize BSC compared to the MC implies a special role with respect to fixation of CO 2 by the Calvin cycle (Takabayashi et al, 2005, Majeran et al, 2008, Friso et al, 2010. However, interpretations differ as to the nature of this role.…”

“…S1; Edwards 2000, 2009;Takabayashi et al, 2005). The Laisk-Edwards model postulates a channeled NDH-catalyzed reduction of PQ by NADPH produced by ME turnover.…”

“…Takabayashi et al (2005) proposed that an NDH-dependent cyclic electron transport pathway and associated Q-cycle turnover was the preferred means of producing adequate ATP for CO 2 fixation in the maize BSC as opposed to the conventional cyclic pathway involving reduction of PQ by Fd 2 . In contrast, the model proposed by Edwards (2000, 2009) envisions linear BSC electron flow from MAL-derived NADPH, via PSI, to a separate NADP pool used by the Calvin cycle (Supplemental Fig.…”

The Operation of Two Decarboxylases, Transamination, and Partitioning of C4 Metabolic Processes between Mesophyll and Bundle Sheath Cells Allows Light Capture To Be Balanced for the Maize C4 Pathway

“…In fact, increasing ATP production at the electron transport chain level would require light (Takabayashi et al, 2005;Kramer and Evans, 2011), whose availability is not under metabolic control. At the same time, the electron transport-mediated dark production of ATP (Morstadt et al, 2002;Bukhov and Carpentier, 2004;Egorova and Bukhov, 2004;Kuntz, 2004) has low conversion efficiency (Kramer and Evans, 2011); hence, an engagement of ATP chemiosynthesis would be incompatible with the observed pattern of J ATP /GA.…”