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Modulating the Activities of Chloroplasts and Mitochondria Promotes Adenosine Cambridge.Org/Qpb Triphosphate Production and Plant Growth

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Modulating the Activities of Chloroplasts and Mitochondria Promotes Adenosine Cambridge.Org/Qpb Triphosphate Production and Plant Growth “QPB-Driver” — 2021/4/30 — 13:11 — page 1 — #1 Quantitative Plant Biology Modulating the activities of chloroplasts and mitochondria promotes adenosine cambridge.org/qpb triphosphate production and plant growth 1 1 1 1 1 Original Research Article Chia P. Voon , Yee-Song Law , Xiaoqian Guan , Shey-Li Lim , Zhou Xu , Wing-Tung Chu1, Renshan Zhang1, Feng Sun1, Mathias Labs2, Dario Leister2, Mathias Pribil3, Cite this article: Chia P. Voon et al. Modulating 4 4 5,6 5,6 7 the activities of chloroplasts and mitochondria Marie Hronková ,Jiˇrí Kubásek , Yong Cui , Liwen Jiang , Michito Tsuyama , promotes adenosine triphosphate production 8 9 1,5,6 and plant growth. Quantitative Plant Biology, Per Gardeström , Mikko Tikkanen and Boon L. Lim 2:e7, 1–10 1 2 https://dx.doi.org/10.1017/qpb.2021.7 School of Biological Sciences, e University of Hong Kong, Pokfulam, China; Plant Molecular Biology, Department 3 of Biology, Ludwig-Maximilians-University Munich (LMU), Munich, Germany; Copenhagen Plant Science Centre, 4 Received: 17 November 2020 Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark; Faculty of 5 Revised: 29 March 2021 Science, University of South Bohemia, Ceske Budejovice, Czech Republic; School of Life Sciences, Centre for Cell and Accepted: 31 March 2021 6 Developmental Biology, e Chinese University of Hong Kong, Shatin, China; State Key Laboratory of 7 Agrobiotechnology, e Chinese University of Hong Kong, Shatin, China; Department of Agriculture, Kyushu Keywords: 8 ATP; AtPAP2; chloroplasts; mitochondria; University, Fukuoka, Japan; Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, 9 NADPH; photosynthesis. Sweden; Molecular Plant Biology, Department of Life Technologies, University of Turku, Turku, Finland Author for correspondence: B. L. Lim, E-mail: [email protected] Abstract Chia P. Voon, Yee-Song Law and Xiaoqian Guan contributed equally to this work. Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in Mathias Labs is currently with KWS SAAT SE, chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for Gateway Research Center, St. Louis, Missouri, balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid USA. phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help + chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP , the electron acceptors of the linear electron flow (LEF). A higher rate of ATP and NADPH production from the LEF, a higher capacity of carbon fixation by the Calvin–Benson–Bassham (CBB) cycle and a greater consumption of NADH in mitochondria enhance photosynthesis in the chloroplasts, ATP production in the mitochondria and sucrose synthesis in the cytosol and eventually boost plant growth and seed yields in the overexpression lines. © The Author(s), 2021. Published by Cambridge University Press in association with The John Innes Centre. This is an Open Access article, 1. Introduction distributed under the terms of the Creative Commons Attribution licence In plant cells, chloroplasts convert light energy into chemical energy, and mitochondria consume (http://creativecommons.org/licenses/by/4.0/), the chemical energy to produce ATP. e optimal carbon fixation and plant growth require these which permits unrestricted re-use, distribution, two energy-transforming organelles to perform strictly coordinated actions. Both organelles and reproduction in any medium, provided the original work is properly cited. utilise protein complexes to construct electron transport chains (ETCs), which are responsi- ble for the formation (chloroplasts) or consumption (mitochondria) of reducing equivalents, translocation of protons and the build-up of the proton gradient as a driving force for ATP synthesis. e cooperation between the chloroplasts and mitochondria, which was invented over 1.5 billion years ago, is nowadays much more complicated than the relationship between a supplier and a consumer in modern plant cells (Dutilleul et al., 2003; Noguchi & Yoshida, 2008). In chloroplasts, the linear electron flow (LEF) generates ATP/NADPH at a ratio of approximately 1.28, and the fixation of carbon dioxide consumes ATP/NADPH at a ratio of 1.5 (Allen, 2003; Foyer et al., 2012). erefore, the photosynthetic efficiency requires the production and consumption of ATP and reductants at appropriate ratios in the chloroplasts, and this process is complicated by their fluxes across the chloroplast inner membrane. Our recent study showed that, in order to limit energy expenditure of chloroplasts in the dark, the “QPB-Driver” — 2021/4/30 — 13:11 — page 2 — #2 2 Chia P. Voon et al. importation of cytosolic ATP into mature chloroplasts is negligible medium, which was supplemented with 2% (w/v) sucrose. (Voon et al., 2018;Voon &Lim, 2019). Hence, during photosynthe- Seedlings of similar sizes were transferred to soil under growth −2 −1 sis, the ATP/NADPH ratio can either be balanced by extra ATP pro- chamber conditions (120–150 µmol m s , 16-h photoperiod, ○ duction from the cyclic electron flow (CEF) or the export of excess 22 C). reductants to the cytosol (Sato et al., 2019; Selinski & Scheibe, 2019). In addition, photorespiration also generates a large amount 2.2. Chlorophyll a fluorescence measurement of NADH in mitochondria, and surplus reducing equivalents are exported to the cytosol through the malate–oxaloacetate (OAA) e chlorophyll a fluorescence levels of the Arabidopsis leaves shuttle (Lim et al., 2020). Hence, surplus reducing equivalents (20 days old) were monitored with IMAGING-PAM M-Series Maxi generated during photosynthesis have to be stored as malate in Version (Heinz Walz GmbH, Effeltrich, Germany). e plants were the vacuole (Gerhardt et al., 1987). Light-dependent production of dark-adapted for at least 1 hr before the measurements. Aer the reducing equivalents in mitochondria is supported by the observa- maximum and initial fluorescence (Fm and F0, respectively) were tion that illumination can cause a rapid pH change in the mitochon- determined with a delay of 40 s, the plants were illuminated using drial matrix, which was unseen when 3-(3,4-dichlorophenyl)-1,1- the following light intensities: 0, 81, 145, 186, 281, 335, 461, 701 −2 −1 dimethylurea (DCMU) was applied (Voon et al., 2018). Further- and 926 µmol photon m s . e duration of the illumination of each light intensity was 3 min. A saturation pulse (800 ms, more, when the mitochondrial ETC was interfered by inhibitors, −2 −1 photosynthetic ATP production in stroma was also affected (Voon 2700 µmol photon m s ) was applied at the end of the 3-min et al., 2018). Here, by studying the physiology of transgenic lines illumination. For each light intensity, the photosynthesis param- that overexpress Arabidopsis thaliana purple acid phosphatase 2 eters were calculated using the formulas: Y(II) was calculated as (AtPAP2), we showed that efficient cooperation of chloroplasts and (Fm’ − F) / Fm’; qP was calculated as (Fm’ − F)/(Fm’ − F0’); Non- mitochondria in optimising reductant production in chloroplasts photochemical quenching (NPQ) was calculated as (Fm − Fm’) / Fm’; and consumption in chloroplasts and mitochondria is important electron transport rate (ETR) was calculated as Y(II) × light inten- for enhancing photosynthesis and productivity. sity × 0.5 × absorptivity. Fm’ was the maximal fluorescence of light- AtPAP2 is anchored on the outer membranes of chloroplasts and illuminated plant. F was the current fluorescence yield. F0’ was mitochondria, and plays a role in protein import into these two estimated by F0 /(Fv / Fm + F0 / Fm’) (Oxborough & Baker, 1997). organelles (Law et al., 2015; Sun et al., 2012a; Zhang et al., 2016). e overexpression of AtPAP2 in Arabidopsis thaliana resulted 2.3. Measurements of P700 oxidation in earlier bolting (Supplementary Figure S1 and Supplementary P700 oxidation [Y(ND) = P / PM] was recorded with Dual-PAM- Movie S1), a higher seed yield (+40–50%) and higher leaf sugar 100 (Heinz Walz GmbH). P700 was determined by the difference and ATP levels (Liang et al., 2015;Sunetal., 2013;Sunetal., 2012b). of 875 and 830-nm measuring lights (Klughammer & Schreiber, e overexpression of AtPAP2 also promotes plant growth and seed 2008). ree-week-old plants were illuminated using the following yield of the biofuel crop Camelina sativa (Zhang et al., 2012). Sim- −2 −1 light intensities: 0, 25, 50, 125, 450 and 150 µmol photon m s . ilarly to Toc33/34 and Tom20s, AtPAP2 is anchored onto the outer e duration of the illumination of each light intensity was 5 min, membranes of chloroplasts and mitochondria via its hydrophobic −2 −1 and saturating pulse (800 ms, 8,000 µmol photon m s ) was C-terminal motif (Sun et al., 2012a). AtPAP2 interacts with the applied in 1-min intervals. precursor of the small subunit of RuBisCO (pSSU; Zhang et al., 2016) and the presequences of a number of multiple organellar Measurements of CO assimilation RNA editing factor (pMORF) proteins (Law et al., 2015) and plays 2.4. 2 a role in their import into chloroplasts (Zhang et al., 2016) and e carbon dioxide assimilation in the 20-day-old plants was mea- mitochondria (Law et al., 2015), respectively. Here, we examined sured using the portable photosynthesis system LI-6400XT (LiCor, how AtPAP2 overexpression affects the physiology of chloroplasts Lincoln, Nebraska, USA) and whole plant Arabidopsis chamber and mitochondria and how these two energy-generating organelles 6400-17. e plants were cultivated hydroponically in four-times orchestrate to produce more sugars and ATP in leaf cells. Our diluted Hoagland nutrient solution (plants were fixed in ‘Grodan’- data suggest that the efficiency of photosynthesis is dependent on mineral wool cubes) under growth chamber conditions (irradiation −2 −1 the activities of the mitochondria. Surplus reducing equivalents 120–150 µmol m s , 16/8-h day/night photoperiod, tempera- ○ generated from the LEF have to be exported and dissipated, and ture 22 C).
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