Leaf senescence is a concerted physiological process involving controlled degradation of cellular structures and reallocation of breakdown products to other plant organs. It is accompanied by increased production of reactive oxygen species (ROS) that are proposed to signal cell death, although both the origin and the precise role of ROS in the execution of this developmental program are still poorly understood. To investigate the contribution of chloroplast-associated ROS to natural leaf senescence, we used tobacco plants expressing a plastid-targeted flavodoxin, an electron shuttle flavoprotein present in prokaryotes and algae. When expressed in plants, flavodoxin specifically prevents ROS formation in chloroplasts during stress situations. Senescence symptoms were significantly mitigated in these transformants, with decreased accumulation of chloroplastic ROS and differential preservation of chlorophylls, carotenoids, protein contents, cell and chloroplast structures, membrane integrity and cell viability. Flavodoxin also improved maintenance of chlorophyll-protein complexes, photosynthetic electron flow, CO2 assimilation, central metabolic routes and levels of bioactive cytokinins and auxins in aging leaves. Delayed induction of senescence-associated genes indicates that the entire genetic program of senescence was affected by flavodoxin. The results suggest that ROS generated in chloroplasts are involved in the regulation of natural leaf senescence.

Instituto de Biología Molecular y Celular de Rosario Facultad de Ciencias Bioquímicas y Farmacéuticas Universidad Nacional de Rosario Rosario Argentina

Instituto de Fisiología Vegetal La Plata Argentina

Leibniz Institute of Plant Genetics and Crop Plant Research OT Gatersleben Seeland Germany

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology Masaryk University Brno Czechia

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Abbasi A. R., Saur A., Hennig P., Tschiersch H., Hajirezaei M.-R., Hofius D., et al. (2009). Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence. Plant Cell. Environ. 32 144–157. 10.1111/j.1365-3040.2008.01907.x PubMed DOI

Almoguera C., Personat J.-M., Prieto-Dapena P., Jordano J. (2015). Heat shock transcription factors involved in seed desiccation tolerance and longevity retard vegetative senescence in transgenic tobacco. Planta 242 461–475. 10.1007/s00425-015-2336-y PubMed DOI

Ambastha V., Tripathy B. C., Tiwari B. S. (2015). Programmed cell death in plants: a chloroplastic connection. Plant Signal. Behav. 10:e989752. PubMed PMC

Antonietta M., Acciaresi H., Guiamet J. (2016). Responses to N deficiency in stay green and non-stay green argentinean hybrids of maize. J. Agron. Crop Sci. 202 231–242. 10.1111/jac.12136 DOI

Ávila-Ospina L., Moison M., Yoshimoto K., Masclaux-Daubresse C. (2014). Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot. 65 3799–3811. 10.1093/jxb/eru039 PubMed DOI

Ay N., Janack B., Humbeck K. (2014). Epigenetic control of plant senescence and linked processes. J. Exp. Bot. 65 3875–3887. 10.1093/jxb/eru132 PubMed DOI

Baker C. J., Mock N. M. (1994). An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue. Plant Cell Tissue Organ Cult. 39 7–12. 10.1007/BF00037585 DOI

Baker N. R. (2008). Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59 89–113. 10.1146/annurev.arplant.59.032607.092759 PubMed DOI

Bernard S. M., Habash D. Z. (2009). The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol. 182 608–620. 10.1111/j.1469-8137.2009.02823.x PubMed DOI

Bernstein N., Shoresh M., Xu Y., Huang B. (2010) Involvement of the plant antioxidative response in the differential growth sensitivity to salinity of leaves vs roots during cell development. Free Radic. Biol. Med. 49 1161–1171. 10.1016/j.freeradbiomed.2010.06.032 PubMed DOI

Biswas M. S., Mano J. I. (2015). Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants. Plant Physiol. 168 885–898. 10.1104/pp.115.256834 PubMed DOI PMC

Bradford M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 248–254. 10.1016/0003-2697(76)90527-3 PubMed DOI

Carrión C. A., Costa M. L., Martínez D. E., Mohr C., Humbeck K., Guiamet J. J. (2013) In vivo inhibition of cysteine proteases provides evidence for the involvement of ‘senescence-associated vacuoles’ in chloroplast protein degradation during dark-induced senescence of tobacco leaves. J. Exp. Bot. 64 4967–4980. 10.1093/jxb/ert285 PubMed DOI

Ceccoli R. D., Blanco N. E., Segretin M. E., Melzer M., Hanke G. T., Scheibe R., et al. (2012). Flavodoxin displays dose-dependent effects on photosynthesis and stress tolerance when expressed in transgenic tobacco plants. Planta 236 1447–1458. 10.1007/s00425-012-1695-x PubMed DOI

Circu M. L., Aw T. Y. (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 48 749–762. 10.1016/j.freeradbiomed.2009.12.022 PubMed DOI PMC

Edlund E., Novak O., Karady M., Ljung K., Jansson S. (2017). Contrasting patterns of cytokinins between years in senescing aspen leaves. Plant Cell Environ. 40 622–634. 10.1111/pce.12899 PubMed DOI

Foyer C. H., Noctor G., Hodges M. (2011). Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J. Exp. Bot. 62 1467–1482. 10.1093/jxb/erq453 PubMed DOI

Fuchs Y., Steller H. (2011). Programmed cell death in animal development and disease. Cell 147 742–758. 10.1016/j.cell.2011.10.033 PubMed DOI PMC

Garapati P., Xue G.-P., Munné-Bosch S., Balazadeh S. (2015). Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol. 168 1122–1139. 10.1104/pp.15.00567 PubMed DOI PMC

Gepstein S., Glick B. R. (2013). Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol. Biol. 82 623–633. 10.1007/s11103-013-0038-z PubMed DOI

Ghaffari M. R., Shahinnia F., Usadel B., Junker B., Schreiber F., Sreenivasulu N., et al. (2016). The metabolic signature of biomass formation in barley. Plant Cell Physiol. 57 1943–1960. 10.1093/pcp/pcw117 PubMed DOI

Golczyk H., Greiner S., Wanner G., Weihe A., Bock R., Börner T., et al. (2014). Chloroplast DNA in mature and senescing leaves: a reappraisal. Plant Cell 26 847–854. 10.1105/tpc.113.117465 PubMed DOI PMC

Gou J. Y., Li K., Wu K., Wang X., Lin H., Cantu D., et al. (2015). Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell 27 1755–1770. 10.1105/tpc.114.134296 PubMed DOI PMC

Goupil P., Benouaret R., Charrier O., Ter Halle A., Richard C., Eyheraguibel B., et al. (2012). Grape marc extract acts as elicitor of plant defence responses. Ecotoxicology 21 1541–1549. 10.1007/s10646-012-0908-1 PubMed DOI

Gregersen P. L., Culetic A., Boschian L., Krupinska K. (2013). Plant senescence and crop productivity. Plant Mol. Biol. 82 603–622. 10.1007/s11103-013-0013-8 PubMed DOI

Guiamet J. J., Tyystjärvi E., Tyystjärvi T., John I., Kairavuo M., Pichersky E., et al. (2002). Photoinhibition and loss of photosystem II reaction centre proteins during senescence of soybean leaves. Enhancement of photoinhibition by the ‘stay-green’mutation cytG. Physiol. Plant. 115 468–478. 10.1034/j.1399-3054.2002.1150317.x PubMed DOI

Hajirezaei M.-R., Peisker M., Tschiersch H., Palatnik J. F., Valle E. M., Carrillo N., et al. (2002). Small changes in the activity of chloroplastic NADP+-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants. Plant J. 29 281–293. 10.1046/j.0960-7412.2001.01209.x PubMed DOI

Havé M., Marmagne A., Chardon F., Masclaux-Daubresse C. (2016). Nitrogen remobilisation during leaf senescence: lessons from Arabidopsis to crops. J. Exp. Bot. 68 2513–2529. 10.1093/jxb/erw365 PubMed DOI

Hirose N., Takei K., Kuroha T., Kamada-Nobusada T., Hayashi H., Sakakibara H. (2007). Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 59 75–83. 10.1093/jxb/erm157 PubMed DOI

Jajic I., Sarna T., Strzalka K. (2015). Senescence, stress, and reactive oxygen species. Plants 4 393–411. 10.3390/plants4030393 PubMed DOI PMC

Jibran R., Hunter D. A., Dijkwel P. P. (2013). Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 82 547–561. 10.1007/s11103-013-0043-2 PubMed DOI

John I., Hackett R., Cooper W., Drake R., Farrell A., Grierson D. (1997). Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol. Biol. 33 641–651. 10.1023/A:1005746831643 PubMed DOI

Juvany M., Müller M., Munné-Bosch S. (2013). Photo-oxidative stress in emerging and senescing leaves: a mirror image? J. Exp. Bot. 64 3087–3098. 10.1093/jxb/ert174 PubMed DOI

Kim J. I., Murphy A. S., Baek D., Lee S.-W., Yun D.-J., Bressan R. A., et al. (2011). YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 62 3981–3992. 10.1093/jxb/err094 PubMed DOI PMC

Kraner M. E., Link K., Melzer M., Ekici A. B., Uebe S., Tarazona P., et al. (2017). Choline transporter-like1 (CHER1) is crucial for plasmodesmata maturation in Arabidopsis thaliana. Plant J. 89 394–406. 10.1111/tpj.13393 PubMed DOI

Li L., Zhao J., Zhao Y., Lu X., Zhou Z., Zhao C., et al. (2016). Comprehensive investigation of tobacco leaves during natural early senescence via multi-platform metabolomics analyses. Sci. Rep. 6:37976. 10.1038/srep37976 PubMed DOI PMC

Li Z., Yuan S., Jia H., Gao F., Zhou M., Yuan N., et al. (2017). Ectopic expression of a cyanobacterial flavodoxin in creeping bentgrass impacts plant development and confers broad abiotic stress tolerance. Plant Biotechnol. J. 15 433–446. 10.1111/pbi.12638 PubMed DOI PMC

Lichtenthaler H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148 350–382. 10.1016/0076-6879(87)48036-1 DOI

Lima A., Durán R., Schujman G. E., Marchissio M. J., Portela M. M., Obal G., et al. (2011). Serine/threonine protein kinase PrkA of the human pathogen Listeria monocytogenes: biochemical characterization and identification of interacting partners through proteomic approaches. J. Proteomics 74 1720–1734. 10.1016/j.jprot.2011.03.005 PubMed DOI

Masclaux C., Valadier M.-H., Brugière N., Morot-Gaudry J.-F., Hirel B. (2000). Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211 510–518. 10.1007/s004250000310 PubMed DOI

McCabe M. S., Garratt L. C., Schepers F., Jordi W. J., Stoopen G. M., Davelaar E., et al. (2001). Effects of PSAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol. 127 505–516. 10.1104/pp.010244 PubMed DOI PMC

Mignolet-Spruyt L., Xu E., Idänheimo N., Hoeberichts F. A., Mühlenbock P., Brosché M., et al. (2016). Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 67 3831–3844. 10.1093/jxb/erw080 PubMed DOI

Moschen S., Higgins J., Di Rienzo J. A., Heinz R. A., Paniego N., Fernández P. (2016). Network and biosignature analysis for the integration of transcriptomic and metabolomic data to characterize leaf senescence process in sunflower. BMC Bioinformatics 17(Suppl. 5):174. 10.1186/s12859-016-1045-2 PubMed DOI PMC

Muñoz P., Munné-Bosch S. (2018). Photo-oxidative stress during leaf, fower and fruit development. Plant Physiol. 176 1004–1014. 10.1104/pp.17.01127 PubMed DOI PMC

Nath K., Phee B.-K., Jeong S., Lee S. Y., Tateno Y., Allakhverdiev S. I., et al. (2013). Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana. Photosynth. Res. 117 547–556. 10.1007/s11120-013-9906-2 PubMed DOI

Niewiadomska E., Polzien L., Desel C., Rozpadek P., Miszalski Z., Krupinska K. (2009). Spatial patterns of senescence and development-dependent distribution of reactive oxygen species in tobacco (Nicotiana tabacum) leaves. J. Plant Physiol. 166 1057–1068. 10.1016/j.jplph.2008.12.014 PubMed DOI

Nimmo H. G. (2003). Control of the phosphorylation of phosphoenolpyruvate carboxylase in higher plants. Arch. Biochem. Biophys. 414 189–196. 10.1016/S0003-9861(03)00115-2 PubMed DOI

Noctor G., Foyer C. H. (2016). Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol. 171 1581–1592. 10.1104/pp.16.00346 PubMed DOI PMC

Penfold C. A., Buchanan-Wollaston V. (2014). Modelling transcriptional networks in leaf senescence. J. Exp. Bot. 65 3859–3873. 10.1093/jxb/eru054 PubMed DOI

Pierella Karlusich J. J., Lodeyro A. F., Carrillo N. (2014). The long goodbye: the rise and fall of flavodoxin during plant evolution. J. Exp. Bot. 65 5161–5178. 10.1093/jxb/eru273 PubMed DOI PMC

Pierella Karlusich J. J., Ceccoli R. D., Graña M., Romero H., Carrillo N. (2015). Environmental selection pressures related to iron utilization are involved in the loss of the flavodoxin gene from the plant genome. Genome Biol. Evol. 7 750–767. 10.1093/gbe/evv031 PubMed DOI PMC

Pierella Karlusich J. J., Zurbriggen M. D., Shahinnia F., Sonnewald S., Sonnewald U., Hosseini S. A., et al. (2017). Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. vesicatoria. Front. Plant Sci. 8:1158. 10.3389/fpls.2017.01158 PubMed DOI PMC

Rasmussen A., Hosseini S. A., Hajirezaei M.-R., Druege U., Geelen D. (2014). Adventitious rooting declines with the vegetative to reproductive switch and involves a changed auxin homeostasis. J. Exp. Bot. 66 1437–1452. 10.1093/jxb/eru499 PubMed DOI PMC

Rhoads D. M., Umbach A. L., Subbaiah C. C., Siedow J. N. (2006). Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141 357–366. 10.1104/pp.106.079129 PubMed DOI PMC

Rivas-San Vicente M., Plasencia J. (2011). Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62 3321–3338. 10.1093/jxb/err031 PubMed DOI

Rogers H., Munné-Bosch S. (2016). Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: similar but different. Plant Physiol. 171 1560–1568. 10.1104/pp.16.00163 PubMed DOI PMC

Rossi F. R., Krapp A. R., Bisaro F., Maiale S. J., Pieckenstain F. L., Carrillo N. (2017). Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J. 95 761–773. 10.1111/tpj.13718 PubMed DOI

Samuilov V. D., Lagunova E. M., Kiselevsky D. B., Dzyubinskaya E. V., Makarova Y. V., Gusev M. V. (2003). Participation of chloroplasts in plant apoptosis. Biosci. Rep. 23 103–117. 10.1023/A:1025576307912 PubMed DOI

Sárvári É, Nyitrai P. (1994). Separation of chlorophyll-protein complexes by deriphat polyacrylamide gradient gel electrophoresis. Electrophoresis 15 1068–1071. 10.1002/elps.11501501159 PubMed DOI

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 676–682. 10.1038/nmeth.2019 PubMed DOI PMC

Schippers J. H., Schmidt R., Wagstaff C., Jing H.-C. (2015). Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol. 169 914–930. 10.1104/pp.15.00498 PubMed DOI PMC

Schmidt G. W., Delaney S. K. (2010). Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol. Genet. Genomics 283 233–241. 10.1007/s00438-010-0511-1 PubMed DOI

Sedigheh H. G., Mortazavian M., Norouzian D., Atyabi M., Akbarzadeh A., Hasanpoor K., et al. (2011). Oxidative stress and leaf senescence. BMC Res. Notes 4:477. 10.1186/1756-0500-4-477 PubMed DOI PMC

Sewelam N., Kazan K., Schenk P. M. (2016). Global plant stress signaling: reactive oxygen species at the cross-road. Front. Plant Sci. 7:187. 10.3389/fpls.2016.00187 PubMed DOI PMC

Shimoda Y., Ito H., Tanaka A. (2016). Arabidopsis STAY-GREEN, Mendel’s green cotyledon gene, encodes magnesium-dechelatase. Plant Cell 28 2147–2160. 10.1105/tpc.16.00428 PubMed DOI PMC

Šmehilová M., Dobrùšková J., Novák O., Takáè T., Galuszka P. (2016). Cytokinin-specific glycosyltransferases possess different roles in cytokinin homeostasis maintenance. Front. Plant Sci. 7:1264. 10.3389/fpls.2016.01264 PubMed DOI PMC

Steponkus P. L., Lanphear F. (1967). Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol. 42 1423–1426. 10.1104/pp.42.10.1423 PubMed DOI PMC

Talla S. K., Panigrahy M., Kappara S., Nirosha P., Neelamraju S., Ramanan R. (2016). Cytokinin delays dark-induced senescence in rice by maintaining the chlorophyll cycle and photosynthetic complexes. J. Exp. Bot. 67 1839–1851. 10.1093/jxb/erv575 PubMed DOI PMC

Thomas H., Howarth C. J. (2000). Five ways to stay green. J. Exp. Bot. 51 329–337. 10.1093/jexbot/51.suppl_1.329 PubMed 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

Tognetti V. B., Mühlenbock P., Van Breusegem F. (2012). Stress homeostasis: the redox and auxin perspective. Plant Cell Environ. 35 321–333. 10.1111/j.1365-3040.2011.02324.x PubMed DOI

Uzelac B., Janoševiæ D., Simonoviæ A., Motyka V., Dobrev P. I., Budimir S. (2016). Characterization of natural leaf senescence in tobacco (Nicotiana tabacum) plants grown in vitro. Protoplasma 253 259–275. 10.1007/s00709-015-0802-9 PubMed DOI

Van Aken O., Van Breusegem F. (2015). Licensed to kill: mitochondria, chloroplasts, and cell death. Trends Plant Sci. 20 754–766. 10.1016/j.tplants.2015.08.002 PubMed DOI

Van Breusegem F., Dat J. F. (2006). Reactive oxygen species in plant cell death. Plant Physiol. 141 384–390. 10.1104/pp.106.078295 PubMed DOI PMC

Wang S., Blumwald E. (2014). Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell 26 4875–4888. 10.1105/tpc.114.133116 PubMed DOI PMC

Wang J., Leister D., Bolle C. (2015). Photosynthetic lesions can trigger accelerated senescence in Arabidopsis thaliana. J. Exp. Bot. 66 6891–6903. 10.1093/jxb/erv393 PubMed DOI PMC

Watanabe M., Balazadeh S., Tohge T., Erban A., Giavalisco P., Kopka J., et al. (2013). Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol. 162 1290–1310. 10.1104/pp.113.21738 PubMed DOI PMC

Wingler A., Lea P. J., Quick W. P., Leegood R. C. (2000). Photorespiration: metabolic pathways and their role in stress protection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 1517–1529. 10.1098/rstb.2000.0712 PubMed DOI PMC

Wu A., Allu A. D., Garapati P., Siddiqui H., Dortay H., Zanor M.-I., et al. (2012). JUNGBRUNNEN1, a reactive oxygen species–responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24 482–506. 10.1105/tpc.111.090894 PubMed DOI PMC

Xie Y., Huhn K., Brandt R., Potschin M., Bieker S., Straub D., et al. (2014). REVOLUTA and WRKY53 connect early and late leaf development in Arabidopsis. Development 141 4772–4783. 10.1242/dev.117689 PubMed DOI PMC

Zapata J., Guera A., Esteban-Carrasco A., Martin M., Sabater B. (2005). Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ. 12 1277–1284. 10.1038/sj.cdd.4401657 PubMed DOI

Zentgraf U. (2007) “Oxidative stress and leaf senescence,” in Annual Plant Reviews, Senescence Processes in Plants, vol. 26 ed. Gang S. (Hoboken, NJ: Blackwell Publishing Ltd.), 69–86.

Zhang H., Zhou C. (2013). Signal transduction in leaf senescence. Plant Mol. Biol. 82 539–545. 10.1007/s11103-012-9980-4 PubMed DOI

Zhang K., Halitschke R., Yin C., Liu C., Gan S. (2013). Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc. Natl. Acad. Sci. U.S.A. 110 14807–14812. 10.1073/pnas.1302702110 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

Plastid-Targeted Cyanobacterial Flavodiiron Proteins Maintain Carbohydrate Turnover and Enhance Drought Stress Tolerance in Barley