Inactivation of mitochondrial complex I stimulates chloroplast ATPase inPhyscomitrium patens

Abstract

Light is the ultimate source of energy for photosynthetic organisms, but respiration is fundamental for supporting metabolism during the night or in heterotrophic tissues. In this work, we isolated Physcomitrella (Physcomitrium patens) plants with altered respiration by inactivating Complex I of the mitochondrial electron transport chain by independent targeting of two essential subunits. Inactivation of Complex I caused a strong growth impairment even in fully autotrophic conditions in tissues where all cells are photosynthetically active, demonstrating that respiration is essential for photosynthesis. Complex I mutants showed alterations in the stoichiometry of respiratory complexes while the composition of photosynthetic apparatus was substantially unaffected. Complex I mutants showed altered photosynthesis with high activity of both Photosystem I and II, likely the result of high chloroplast ATPase activity that led to smaller ΔpH formation across thylakoid membranes, decreasing photosynthetic control on cytochrome b6f in Complex I mutants. These results demonstrate that alteration of respiratory activity directly impacts photosynthesis in P. patens and that metabolic interaction between organelles is essential in their ability to use light energy for growth.

Inactivation of mitochondrial complex IV inPhyscomitrium patensreveals the essential role of respiration in coordinating plants metabolism

“…A similar effect has been shown in tobacco plants depleted in complex I activity, where the remodulation of electron transport increased the efficiency of oxidative phosphorylation, so that the predicted ATP production was maintained (Vidal et al, 2007). More recently, we similarly observed in P. patens complex I mutants increased chloroplast ATPase activity to maintain ATP leaves (Mellon et al, 2021). cox11 plants are substantially unaltered in the light reactions of photosynthesis and thus are able to exploit light energy for synthesis of ATP and NADPH.…”

“…Remarkably, plants with altered complex I activity, including P. patens, commonly show AOX overaccumulation, which is not the case here (Fromm, Senkler, et al, 2016;Gutierres et al, 1997;Mellon et al, 2021;Meyer et al, 2009;Pétriacq et al, 2017;Sabar et al, 2000). AOX overaccumulation in these plants, however, is associated with the induction of mitochondrial retrograde signalling (Giraud et al, 2009;Millar et al, 2011), which is likely not occurring in cox11 plants here.…”

“…This contrasts with respiratory mutants depleted in complex IV in the green alga Chlamydomonas reinhardtii, which showed a growth delay only when grown under hetero/mixotrophic conditions but were not significantly different from the WT in minimal medium when photosynthesis was active (Colin et al, 1995). This suggests that the role of respiration in photosynthetic organisms changed during plants evolution (Mellon et al, 2021).…”

“…Protein extraction and immunoblotting was performed as described previously (Mellon et al, 2021). Samples were loaded so that the same amount of chlorophylls was present.…”

“…A major limitation in advancing knowledge in this area has been the lack of viable land plant mutants with depleted respiration. While there is a collection of mutants depleted in one or more respiratory complexes in the green alga Chlamydomonas reinhardtii , as reviewed by Salinas et al, 2014, complete knockout mutants in land plants are only available for complex I in Arabidopsis thaliana (Fromm, Braun, et al, 2016; Meyer et al, 2009; Pétriacq et al, 2017), Nicotiana sylvestris (Brangeon et al, 2000; Gutierres et al, 1997), and the moss Physcomitrium patens (Mellon et al, 2021). Full knockout mutants for complexes II-V have never been isolated in seed plants because of the negative effects on embryo development and seed germination.…”