Plastid-Targeted Cyanobacterial Flavodiiron Proteins Maintain Carbohydrate Turnover and Enhance Drought Stress Tolerance in Barley
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33519872
PubMed Central
PMC7838373
DOI
10.3389/fpls.2020.613731
Knihovny.cz E-zdroje
- Klíčová slova
- Hordeum vulgare L., biomass, metabolites, photosynthesis, plastid biotechnology, yield,
- Publikační typ
- časopisecké články MeSH
Chloroplasts, the sites of photosynthesis in higher plants, have evolved several means to tolerate short episodes of drought stress through biosynthesis of diverse metabolites essential for plant function, but these become ineffective when the duration of the stress is prolonged. Cyanobacteria are the closest bacterial homologs of plastids with two photosystems to perform photosynthesis and to evolve oxygen as a byproduct. The presence of Flv genes encoding flavodiiron proteins has been shown to enhance stress tolerance in cyanobacteria. In an attempt to support the growth of plants exposed to drought, the Synechocystis genes Flv1 and Flv3 were expressed in barley with their products being targeted to the chloroplasts. The heterologous expression of both Flv1 and Flv3 accelerated days to heading, increased biomass, promoted the number of spikes and grains per plant, and improved the total grain weight per plant of transgenic lines exposed to drought. Improved growth correlated with enhanced availability of soluble sugars, a higher turnover of amino acids and the accumulation of lower levels of proline in the leaf. Flv1 and Flv3 maintained the energy status of the leaves in the stressed plants by converting sucrose to glucose and fructose, immediate precursors for energy production to support plant growth under drought. The results suggest that sugars and amino acids play a fundamental role in the maintenance of the energy status and metabolic activity to ensure growth and survival under stress conditions, that is, water limitation in this particular case. Engineering chloroplasts by Flv genes into the plant genome, therefore, has the potential to improve plant productivity wherever drought stress represents a significant production constraint.
Zobrazit více v PubMed
Ahkami A. H., Melzer M., Ghaffari M. R., Pollmann S., Ghorbani Javid M., Shahinnia F., et al. (2013). Distribution of indole-3-acetic acid in Petunia hybrida shoot tip cuttings and relationship between auxin transport, carbohydrate metabolism and adventitious root formation. Planta 238 499–517. 10.1007/s00425-013-1907-z PubMed DOI PMC
Alegre L. (2004). Review: Die and let live: leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol. 31 203–216. 10.1071/fp03236 PubMed DOI
Allahverdiyeva Y., Ermakova M., Eisenhut M., Zhang P., Richaud P., Hagemann M., et al. (2011). Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J. Biol. Chem. 286 24007–24014. 10.1074/jbc.M111.223289 PubMed DOI PMC
Allahverdiyeva Y., Isojärvi J., Zhang P., Aro E. M. (2015a). Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5 716–743. 10.3390/life5010716 PubMed DOI PMC
Allahverdiyeva Y., Mustila H., Ermakova M., Bersanini L., Richaud P., Ajlani G., et al. (2013). Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc. Natl. Acad. Sci. U. S. A. 110 4111–4116. 10.1073/pnas.1221194110 PubMed DOI PMC
Allahverdiyeva Y., Suorsa M., Tikkanen M., Aro E. M. (2015b). Photoprotection of photosystems in fluctuating light intensities. J. Exp. Bot. 66 2427–2436. 10.1093/jxb/eru463 PubMed DOI
Atkinson D. E., Walton G. M. (1967). Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J. Biol. Chem. 242 3239–3241. PubMed
Brestic M., Cornic G., Fryer M. J., Baker N. R. (1995). Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196 450–457. 10.1007/BF00203643 DOI
Couée I., Sulmon C., Gouesbet G., Amrani A. E. I. (2006). Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Expt. Bot. 57 449–459. 10.1093/jxb/erj027 PubMed DOI
Counce P. A., Gravois K. A. (2006). Sucrose synthase activity as a potential indicator of high rice grain yield. Crop Sci. 46 1501–1507. 10.2135/cropsci2005.0240 DOI
Cruz de Carvalho M. H. (2008). Drought stress and reactive oxygen species: production, scavenging and signalling. Plant Signal. Behav. 3 156–165. 10.4161/psb.3.3.5536 PubMed DOI PMC
Dang K. V., Plet J., Tolleter D., Jokel M., Cuiné S., Carrier P., et al. (2014). Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 26 3036–3035. 10.1105/tpc.114.126375 PubMed DOI PMC
Das A., Rushton P. J., Rohila J. S. (2017). Metabolomic profiling of soybeans (Glycine max L.) reveals the importance of sugar and nitrogen metabolism under drought and heat stress. Plants 6:21. 10.3390/plants6020021 PubMed DOI PMC
Ebrahim F., Arzani A., Peng J. (2020). Salinity tolerance of wild barley Hordeum vulgare ssp. Spontaneum. Plant Breed. 139 304–316. 10.1111/pbr.12770 DOI
Fàbregas N., Fernie A. R. (2019). The metabolic response to drought. J. Exp. Bot. 70 1077–1085. 10.1093/jxb/ery437 PubMed DOI
Fàbregas N., Lozano-Elena F., Blasco-Escámez D. (2018). Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth. Nat. Commun. 9:4680. 10.1038/s41467-018-06861-3 PubMed DOI PMC
Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S. (2009). Plant drought stress: effects, mechanisms and management. Agron. Sust. Devel. 29 185–212. 10.1051/agro:2008021 DOI
Gan S. (2003). Mitotic and postmitotic senescence in plants. Sci. Aging Knowl. Environ. 24:RE7. 10.1126/sageke.2003.38.re7 PubMed DOI
Gerotto C., Alboresi A., Meneghesso A., Jokel M., Suorsa M., Aro E. M., et al. (2016). Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc. Natl. Acad. Sci. U. S. A. 113 12322–12327. 10.1073/pnas.1606685113 PubMed DOI PMC
Gómez R., Carrillo N., Morelli M. P., Tula S., Shahinnia F., Hajirezaei M. R., et al. (2018). Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts. Photosynth. Res. 136 129–138. 10.1007/s11120-017-0449-9 PubMed DOI
Gómez R., Vicino P., Carrillo N., Lodeyro A. F. (2019). Manipulation of oxidative stress responses as a strategy to generate stress–tolerant crops. From damage to signaling to tolerance. Crit. Rev. Biotechnol. 39 693–708. 10.1080/07388551.2019.1597829 PubMed DOI
Guo R., Shi L. X., Jiao Y., Li M. X., Zhong X. L., Gu F. X., et al. (2018). Metabolic responses to drought stress in the tissues of drought-tolerant and drought–sensitive wheat genotype seedlings. AoB Plants 10:ly016. 10.1093/aobpla/ply016 PubMed DOI PMC
Haink G., Deussen A. (2003). Liquid chromatography method for the analysis of adenosine compounds. J. Chromatogr. 784 189–193. 10.1016/s1570-0232(02)00752-3 PubMed DOI
Haupt-Herting S., Fock H. P. (2002). Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann. Bot. 89 851–859. 10.1093/aob/mcf023 PubMed DOI PMC
Helman Y., Tchernov D., Reinhold L., Shibata M., Ogawa T., Schwarz R., et al. (2003). Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr. Biol. 13 230–235. 10.1016/S0960-9822(03)00046-0 PubMed DOI
Hildebrandt T. M., Nunes Nesi A., Araujo W. L., Braun H. P. (2015). Amino acid catabolism in plants. Mol. Plant. 8 1563–1579. 10.1016/j.molp.2015.09.005 PubMed DOI
Hodaei M., Rahimmalek M., Arzani A., Talebi M. (2018). The effect of water stress on phytochemical accumulation, bioactive compounds and expression of key genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Ind. Crops Prod. 120 295–304. 10.1016/j.indcrop.2018.04.073 DOI
Kaur G., Asthir B. (2015). Proline: a key player in plant abiotic stress tolerance. Biol. Plant. 59 609–619. 10.1007/s10535-015-0549-3 DOI
Kovalchuk N., Jia W., Eini O., Morran S., Pyvovarenko T., Fletcher S., et al. (2013). Optimization of TaDREB3 gene expression in transgenic barley using cold-inducible promoters. Plant Biotechnol. J. 11 659–670. 10.1111/pbi.12056 PubMed DOI
Lawlor D. W. (1995). “Effects of water deficit on photosynthesis,” in Environment and Plant Metabolism: Flexibility and Acclimation, ed. Smirnoff N., (Oxford:BIOS Scientific Publishers Limited; ), 129–160.
Lawlor D. W., Tezara W. (2009). Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Annals Bot. 103 561–579. 10.1093/aob/mcn244 PubMed DOI PMC
Li Z., Hansen J. L., Liu Y., Zemetra R. S., Berger P. H. (2004). Using real−time PCR to determine transgene copy number in wheat. Plant Mol. Biol. Rep. 22 179–188. 10.1007/BF02772725 DOI
Logemann J., Schell J., Willmitzer L. (1987). Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163 16–20. 10.1016/0003-2697(87)90086-8 PubMed DOI
Lonbani M., Arzani A. (2011). Morpho-physiological traits associated with terminal droughtstress tolerance in triticale and wheat. Agron. Res. 9 315–329.
Marchetti Cintia F., Ugena L., Humplík Jan F., Polák M., Ćavar Zeljković S., Podlešáková K., et al. (2019). A novel image-based screening method to study water-deficit response and recovery of barley populations using canopy dynamics phenotyping and simple metabolite profiling. Front. Plant Sci. 10:1252. 10.3389/fpls.2019.01252 PubMed DOI PMC
Marthe C., Kumlehn J., Hensel G. (2015). Barley (Hordeum vulgare L.) transformation using immature embryos. Methods Mol. Biol. 1223 71–83. 10.1007/978-1-4939-1695-5_6 PubMed DOI
Mayta M. L., Lodeyro A. F., Guiamet J. J., Tognetti V. B., Melzer M., Hajirezaei M. R., et al. (2018). Expression of a plastid-targeted flavodoxin decreases chloroplast reactive oxygen species accumulation and delays senescence in aging tobacco leaves. Front. Plant Sci. 9:1039. 10.3389/fpls.2018.01039 PubMed DOI PMC
Peltier G., Tolleter D., Billon E., Cournac L. (2010). Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106 19–31. 10.1007/s11120-010-9575-3 PubMed DOI
Pires M. V., Pereira Júnior A. A., Medeiros D. B., Daloso D. M., Pham P. A., Barros K. A. (2016). The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis. Plant Cell Environ. 39 1304–1319. 10.1111/pce.12682 PubMed DOI
Price A. H., Cairns J. E., Horton P., Jones H. G., Griffiths H. (2002). Linking drought-resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. J. Exp. Bot. 53 989–1004. 10.1093/jexbot/53.371.989 PubMed DOI
Quick W. P., Chaves M. M., Wendler R., David M., Rodrigues M. L., Passaharinho J. A., et al. (1992). The effect of water stress on photosynthetic carbon metabolisms in four species grown under field conditions. Plant Cell Environ. 15 25–35. 10.1111/j.1365-3040.1992.tb01455.x DOI
Rai V. K., Sharma U. D. (1991). Amino acids can modulate ABA induced stomatal closure, stomatal resistance and K+ fluxes in Vicia faba leaves. Beitr. Biol. Pflanz. 66 393–405. 10.1016/S0015-3796(89)80057-5 DOI
Rutherford A. W., Osyczka A., Rappaport F. (2012). Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett. 586 603–616. 10.1016/j.febslet.2011.12.039 PubMed DOI
Saghai-Maroof M. A., Soliman K. M., Jorgensen R. A., Allard R. W. (1984). Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc. Natl. Acad. Sci. 81 8014–8018. 10.1073/pnas.81.24.8014 PubMed DOI PMC
Saraiva L. M., Vicente J. B., Teixeira M. (2004). The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv. Microb. Physiol. 49 77–129. 10.1016/S0065-2911(04)49002-X PubMed DOI
Schmittgen T. D., Livak K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3 1101–1108. 10.1038/nprot.2008.73 PubMed DOI
Sétif P., Shimakawa G., Krieger-Liszkay A., Miyake C. (2020). Identification of the electron donor to flavodiiron proteins in Synechocystis sp. PCC6803 by in vivo spectroscopy. Biochim. Biophys. Acta Bioenerg. 1861:148256. 10.1016/j.bbabio.2020.148256 PubMed DOI
Shahinnia F., Tula S., Hensel G., Reiahisamani N., Nasr N., Kumlehn J., et al. (2020). Integrating cyanobacterial flavodiiron proteins within the chloroplast photosynthetic electron transport chain maintains carbohydrate turnover and enhances drought stress tolerance in barley. bioRxiv 10.1101/2020.09.29.318394 PubMed DOI PMC
Sharkey T. D., Badger M. R. (1982). Effects of water stress on photosynthetic electron transport, photophosphorylation and metabolite levels of Xanthium strumarium cells. Planta 156 199–206. 10.1007/BF00393725 PubMed DOI
Silaghi-Dumitrescu R., Kurtz D. M., Jr., Ljungdahl L. G., Lanzilotta W. N. (2005). X-ray crystal structures of Moorella thermoacetica FprA. Novel diiron site structure and mechanistic insights into a scavenging nitric oxide reductase. Biochemistry 44 6492–6501. 10.1021/bi0473049 PubMed DOI
Singh M., Kumar J., Singh S., Singh V. P., Prasad S. M. (2015). Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Environ. Sci. Biotechnol. 14 407–426. 10.1007/s11157-015-9372-8 DOI
Song P., Cai C. Q., Skokut M., Kosegi B., Petolino J. (2002). Quantitative real-time PCR as a screening tool for estimating transgene copy number in WHISKERSTM-derived transgenic maize. Plant Cell Rep. 20 948–954. 10.1007/s00299-001-0432-x DOI
Sun X., Wen T. (2011). Physiological roles of plastid terminal oxidase in plant stress responses. J. Biosci. 36 951–956. 10.1007/s12038-011-9161-7 PubMed DOI
Szabados L., Savouré A. (2010). Proline: a multifunctional amino acid. Trends Plant Sci. 15 89–97. 10.1016/j.tplants.2009.11.009 PubMed DOI
Takagi D., Takumi S., Hashiguchi M., Sejima T., Miyake C. (2016). Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol. 171 1626–1634. 10.1104/pp.16.00246 PubMed DOI PMC
Tezara W., Mitchell V. J., Driscoll S. D., Lawlor D. W. (1999). Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401 914–917. 10.1038/44842 DOI
Tognetti V. B., Palatnik J. F., Fillat M. F., Melzer M., Hajirezaei M. R., Valle E. M., et al. (2006). Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell 18 2035–2050. 10.1105/tpc.106.042424 PubMed DOI PMC
Tula S., Shahinnia F., Melzer M., Rutten T., Gómez R., Lodeyro A. F., et al. (2020). Providing an additional electron sink by the introduction of cyanobacterial flavodiirons enhances growth of A. thaliana under various light intensities. Front. Plant Sci. 11 1–12. 10.3389/fpls.2020.00902 PubMed DOI PMC
Wada S., Yamamoto H., Suzuki Y., Yamori W., Shikanai T., Makino A. (2018). Flavodiiron protein substitutes for cyclic electron flow without competing CO2 assimilation in rice. Plant Physiol. 176 1509–1518. 10.1104/pp.17.01335 PubMed DOI PMC
Wang X., Cai J., Jiang D., Liu F., Dai T., Cao W. (2011). Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J. Plant Physiol. 168 585–593. 10.1016/j.jplph.2010.09.016 PubMed DOI
Wasserfallen A., Ragettli S., Jouanneau Y., Leisinger T. (1998). A family of flavoproteins in the domains Archaea and Bacteria. Eur. J. Biochem. 254 325–332. 10.1046/j.1432-1327.1998.2540325.x PubMed DOI
Yamamoto H., Takahashi S., Badger M. R., Shikanai T. (2016). Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat. Plants 2:16012. 10.1038/nplants.2016.12 PubMed DOI
Zadoks J. C., Chang T. T., Konzak C. F. (1974). A decimal code for the growth stages of cereals. Weed Res. 14 415–421. 10.1111/j.1365-3180.1974.tb01084.x DOI
Zhang P., Allahverdiyeva Y., Eisenhut M., Aro E. M. (2009). Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS One 4:e5331. 10.1371/journal.pone.0005331 PubMed DOI PMC
Zurbriggen M. D., Carrillo N., Tognetti V. B., Melzer M., Peisker M., Hause B., et al. (2009). Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 60 962–973. 10.1111/j.1365-313X.2009.04010.x PubMed DOI
Photosystems under high light stress: throwing light on mechanism and adaptation