Does the stromal concentration of P_i control chloroplast ATP synthase protein amount in contrasting growth environments?

References

• Hoefnagel MHN, Atkin OK, Wiskich JT. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta. 1998;1366:1–7. doi:10.1016/S0005-2728(98)00126-1.
   Web of Science ®Google Scholar
• Raghavendra AS, Padmasree K. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 2003;8:546–553. doi:10.1016/j.tplants.2003.09.015.
   PubMed Web of Science ®Google Scholar
• Gardeström P, Igamberdiev AU. The origin of cytosolic ATP in photosynthetic cells. Physiol Plant. 2016;157:367–379. doi:10.1111/ppl.12455.
   PubMed Web of Science ®Google Scholar
• Shameer S, Ratcliffe G, Sweetlove LJ. Leaf energy balance requires mitochondrial respiration and export of chloroplast NADPH in the light. Plant Physiol. 2019;180:1947–1961. doi:10.1104/pp.19.00624.
   PubMed Web of Science ®Google Scholar
• Kramer DM, Evans JR. The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 2011;155:70–78. doi:10.1104/pp.110.166652.
   PubMed Web of Science ®Google Scholar
• Lastdrager J, Hanson J, Smeekens S. Sugar signals and the control of plant growth and development. J Exp Bot. 2014;65:799–807. doi:10.1093/jxb/ert474.
   PubMed Web of Science ®Google Scholar
• Ruan Y-L. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol. 2014;65:33–67. doi:10.1146/annurev-arplant-050213-040251.
   PubMed Web of Science ®Google Scholar
• Griffiths CA, Paul MJ, Foyer CH. Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochim Biophys Acta. 2016;1857:1715–1725. doi:10.1016/j.bbabio.2016.07.007.
   PubMed Web of Science ®Google Scholar
• Stitt M, Lunn J, Usadel B. Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake. Plant J. 2010;61:1067–1091. doi:10.1111/j.1365-313X.2010.04142.x.
   PubMed Web of Science ®Google Scholar
• Lewis CE, Noctor G, Causton D, Foyer CH. Regulation of assimilate partitioning in leaves. Aust J Plant Physiol. 2000;27:507–519.
   Google Scholar
• Paul MJ, Foyer CH. Sink regulation of photosynthesis. J Exp Bot. 2001;52:1383–1400. doi:10.1093/jexbot/52.360.1383.
   PubMed Web of Science ®Google Scholar
• Dong S, Beckles DM. Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J Plant Physiol. 2019;234–235:80–93. doi:10.1016/j.jplph.2019.01.007.
   PubMed Web of Science ®Google Scholar
• McClain AM, Sharkey TD. Triose phosphate utilization and beyond: from photosynthesis to end product synthesis. J Exp Bot. 2019;70:1755–1766. doi:10.1093/jxb/erz058.
   PubMed Web of Science ®Google Scholar
• Plaxton WC, Podesta FE. The functional organization and control of plant respiration. Crit Rev Plant Sci. 2006;25:159–198. doi:10.1080/07352680600563876.
   Web of Science ®Google Scholar
• Millar AH, Whelan J, Soole KL, Day DA. Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol. 2011;62:79–104. doi:10.1146/annurev-arplant-042110-103857.
   PubMed Web of Science ®Google Scholar
• Vanlerberghe GC. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci. 2013;14:6805–6847. doi:10.3390/ijms14046805.
   PubMed Web of Science ®Google Scholar
• Selinski J, Scheibe R, Day DA, Whelan J. Alternative oxidase is positive for plant performance. Trends Plant Sci. 2018;23:588–597. doi:10.1016/j.tplants.2018.03.012.
   PubMed Web of Science ®Google Scholar
• Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot. 2012;63:1637–1661. doi:10.1093/jxb/ers013.
   PubMed Web of Science ®Google Scholar
• Yamori W, Shikanai T. Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol. 2016;67:81–106. doi:10.1146/annurev-arplant-043015-112002.
   PubMed Web of Science ®Google Scholar
• Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006;141:391–396. doi:10.1104/pp.106.082040.
   PubMed Web of Science ®Google Scholar
• Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman F-A. The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu Rev Plant Biol. 2015;66:49–74. doi:10.1146/annurev-arplant-043014-114744.
   PubMed Web of Science ®Google Scholar
• Taniguchi M, Miyake H. Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr Opin Plant Biol. 2012;15:252–260. doi:10.1016/j.pbi.2012.01.014.
   PubMed Web of Science ®Google Scholar
• Vanlerberghe GC, Martyn GD, Dahal K. Alternative oxidase: a respiratory electron transport chain pathway essential for maintaining photosynthetic performance during drought stress. Physiol Plant. 2016;157:322–337. doi:10.1111/ppl.12451.
   PubMed Web of Science ®Google Scholar
• Dahal K, Vanlerberghe GC. Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought. New Phytol. 2017;213:560–571. doi:10.1111/nph.14169.
   PubMed Web of Science ®Google Scholar
• Dahal K, Wang J, Martyn GD, Rahimy F, Vanlerberghe GC. Mitochondrial alternative oxidase maintains respiration and preserves photosynthetic capacity during moderate drought in Nicotiana tabacum. Plant Physiol. 2014;166:1560–1574. doi:10.1104/pp.114.247866.
   PubMed Web of Science ®Google Scholar
• Dahal K, Martyn GD, Vanlerberghe GC. Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink. New Phytol. 2015;208:382–395. doi:10.1111/nph.13479.
   PubMed Web of Science ®Google Scholar
• Dahal K, Vanlerberghe GC. Improved chloroplast energy balance during water deficit enhances plant growth: more crop per drop. J Expt Bot. 2018;69:1183–1197. doi:10.1093/jxb/erx474.
   PubMed Web of Science ®Google Scholar
• Dahal K, Vanlerberghe GC. Growth at elevated CO2 requires acclimation of the respiratory chain to support photosynthesis. Plant Physiol. 2018;178:82–100. doi:10.1104/pp.18.00712.
   PubMed Web of Science ®Google Scholar
• Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM, Schöttler MA. ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell. 2011;23:304–321. doi:10.1105/tpc.110.079111.
   PubMed Web of Science ®Google Scholar
• Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S. The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol. 2011;155:956–962. doi:10.1104/pp.110.168435.
   PubMed Web of Science ®Google Scholar
• Kanazawa A, Kramer DM. In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of ATP synthase. PNAS. 2002;99:12789–12794. doi:10.1073/pnas.182427499.
   PubMed Web of Science ®Google Scholar
• Takizawa K, Kanazawa A, Kramer DM. Depletion of stromal Pi induces high “energy dependent” antenna exciton quenching (qE) by decreasing proton conductivity at CF0-CF1 ATP synthase. Plant Cell Environ. 2008;31:235–243. doi:10.1111/j.1365-3040.2007.01753.x.
   PubMed Web of Science ®Google Scholar
• Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM. Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot. 2005;56:395–406. doi:10.1093/jxb/eri022.
   PubMed Web of Science ®Google Scholar
• Tikhonov AN. pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res. 2013;116:511–534. doi:10.1007/s11120-013-9845-y.
   PubMed Web of Science ®Google Scholar
• Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM. An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell. 2010;22:221–233. doi:10.1105/tpc.109.071084.
   PubMed Web of Science ®Google Scholar
• Sharkey TD, Weise SE. The glucose 6-phosphate shunt around the Calvin-Benson cycle. J Exp Bot. 2016;67:4067–4077. doi:10.1093/jxb/erv484.
   PubMed Web of Science ®Google Scholar
• Li J, Weraduwage SM, Preiser AL, Tietz S, Weise SE, Strand DD, Froehlich JE, Kramer DM, Hu J, Sharkey TD. A cytosolic bypass and G6P shunt in plants lacking peroxisomal hydroxxypyruvate reductase. Plant Physiol. 2019;180:783–792. doi:10.1104/pp.19.00256.
   PubMed Web of Science ®Google Scholar
• Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, Husted S. The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiol. 2018;177:271–284. doi:10.1104/pp.17.01624.
   PubMed Web of Science ®Google Scholar
• Morales A, Yin X, Harbinson J, Driever SM, Molenaar J, Kramer DM, Struik PC. In silico analysis of the regulation of the photosynthetic electron transport chain in C3 plants. Plant Physiol. 2018;176:1247–1261. doi:10.1104/pp.17.00779.
   PubMed Web of Science ®Google Scholar
• Li P, Weng J, Zhang Q, Yu L, Yao Q, Chang L, Niu Q. Physiological and biochemicial responses of Cucumis melo L. chloroplasts to low-phosphate stress. Front Plant Sci. 2018;9:Article 1525. doi:10.3389/fpls.2018.01525.
   PubMed Web of Science ®Google Scholar
• Sharkey TD, Vanderveer PJ. Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol. 1989;91:679–684. doi:10.1104/pp.91.2.679.
   PubMed Web of Science ®Google Scholar
• Kiirats O, Cruz JA, Edwards GE, Kramer DM. Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase. Func Plant Biol. 2009;36:893–901. doi:10.1071/FP09129.
   PubMed Web of Science ®Google Scholar
• Mukherjee P, Banerjee S, Wheeler A, Ratliff LA, Irigoyen S, Garcia LR, Lockless SW, Versaw WK. Live imaging of inorganic phosphate in plants with cellular and subcellular resolution. Plant Physiol. 2015;167:628–638. doi:10.1104/pp.114.254003.
   PubMed Web of Science ®Google Scholar
• Kanno S, Cuyas L, Javot H, Bligny R, Gout E, Dartevelle T, Hanchi M, Nakanishi TM, Thibaud M-C, Nussaume L. Performance and limitations of phosphate quantification: guidelines for plant biologists. Plant Cell Physiol. 2016;57:690–706. doi:10.1093/pcp/pcv208.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Kakizuka A, Imamura H. BTeam, a novel BRET-based biosensor for the accurate quantification of ATP concentration within living cells. Sci Rep. 2016;6:39618. doi:10.1038/srep39618.
   PubMed Web of Science ®Google Scholar
• Voon CP, Guan X, Sun Y, Sahu A, Chan MN, Gardeström P, Wagner S, Fuchs P, Nietzel T, Versaw WK, et al. ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing. PNAS. 2018;115:E10778–E10787. doi:10.1073/pnas.1711497115.
   PubMed Web of Science ®Google Scholar
• Yamori W, Evans JR, Von Caemmerer S. Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation in tobacco leaves. Plant Cell Environ. 2010;33:332–343. doi:10.1111/j.1365-3040.2009.02067.x.
   PubMed Web of Science ®Google Scholar
• Schӧttler MA, Tόth SZ. Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci. 2014;5:Article 188.
   PubMed Web of Science ®Google Scholar
• Yang JT, Preiser AL, Li Z, Weise SE, Sharkey TD. Triose phosphate use limitation of photosynthesis: short-term and long-term effects. Planta. 2016;243:687–698. doi:10.1007/s00425-015-2436-8.
   PubMed Web of Science ®Google Scholar
• Hurry V, Å S, Furbank R, Stitt M. The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. Plant J. 2000;24:383–396. doi:10.1046/j.1365-313x.2000.00888.x.
   PubMed Web of Science ®Google Scholar
• Nielsen TH, Krapp A, Röper-Schwarz U, Stitt M. The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant Cell Environ. 1998;21:443–454. doi:10.1046/j.1365-3040.1998.00295.x.
   Web of Science ®Google Scholar
• Schöttler MA, Tóth SZ, Boulouis A, Kahlau S. Photosynthetic complex stoichiometry dynamics in higher plants: biogenesis, function, and turnover of ATP synthase and cytochrome b6f complex. J Exp Bot. 2015;66:2373–2400. doi:10.1093/jxb/eru495.
   Google Scholar
• Benz M, Bals T, Gügel IL, Piotrowski M, Kuhn A, Schünemann D, Soll J, Ankele E. Alb4 of Arabidopsis promotes assembly and stabilization of a non chlorophyll-binding photosynthetic complex, the CF1CF0-ATP synthase. Mol Plant. 2009;2:1410–1424. doi:10.1093/mp/ssp095.
   PubMed Web of Science ®Google Scholar
• Rühle T, Razeghi JA, Vamvaka E, Viola S, Gandini C, Kleine T, Schünemann D, Barbato R, Jahns P, Leister D. The Arabidopsis protein CONSERVED ONLY IN THE GREEN LINEAGE160 promotes the assembly of the membranous part of the chloroplast ATP synthase. Plant Physiol. 2014;165:207–226. doi:10.1104/pp.114.237883.
   PubMed Web of Science ®Google Scholar
• Fristedt R, Martins NF, Strenkert D, Clarke CA, Suchoszek M, Thiele W, Schöttler MA, Merchant SS. The thylakoid membrane protein CGL160 supports CF1CF0 ATP synthase accumulation in Arabidopsis thaliana. PLoS One. 2015;10:e0121658. doi:10.1371/journal.pone.0121658.
   PubMed Web of Science ®Google Scholar
• Hoshiyasu S, Kohzuma K, Yoshida K, Fujiwara M, Fukao Y, Yokota A, Akashi K. Potential involvement of N-terminal acetylation in the quantitative regulation of the Ε subunit of chloroplast ATP synthase under drought stress. Biosci Biotechnol Biochem. 2013;77:998–1007. doi:10.1271/bbb.120945.
   PubMed Web of Science ®Google Scholar
• Linster E, Wirtz M. N-terminal acetylation: an essential protein modification emerges as an important regulator of stress responses. J Exp Bot. 2018;69:4555–4568.
   PubMed Web of Science ®Google Scholar