Deg proteases play critical roles in photoprotection and PSII-repair circle, which remains elusive in cereal crops including wheat. Here, a Deg7-encoding gene TaDeg7 was silenced in wheat via a Barley stripe mosaic virus-induced gene-silencing system (BSMV-VIGS). When the expression level of TaDeg7 was downregulated, the photosynthetic activity including CO2 assimilation rate, actual photochemical efficiency of PSII, and electron transport rate declined while the nonphotochemical quenching increased significantly. When grown in high light, the BSMV:TaDeg7 plants accumulated more soluble sugar, malondialdehyde, and superoxide anion but had lower superoxide dismutase activity and less ascorbic acid. Additionally, the expression levels of TaPsbA and TarbcS were repressed in the BSMV:TaDeg7 plants in high light. The BSMV:TaDeg7 plants also were more sensitive to high-light stress. Collectively, it appeared that TaDeg7 may be a potential target for wheat radiation-use efficiency improvement against high light stress.

College of Life Sciences Huaibei Normal University 235000 Huaibei China

State Key Laboratory of Plant Cell and Chromosome Engineering Institute of Genetics and Developmental Biology Chinese Academy of Sciences 100101 Beijing China

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Adir N., Zer H., Shochat S., Ohad I.: Photoinhibition – a historical perspective. – Photosynth. Res. 76: 343-370, 2003. 10.1023/A:1024969518145 PubMed DOI

Arnon D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. – Plant Physiol. 24: 1-15, 1949. 10.1104/pp.24.1.1 PubMed DOI PMC

Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. – BBA-Bioenergetics 1143: 113-134, 1993. 10.1016/0005-2728(93)90134-2 PubMed DOI

Baranek M., Wyka T.P., Jackowski G.: Downregulation of chloroplast protease AtDeg5 leads to changes in chronological progression of ontogenetic stages, leaf morphology and chloroplast ultrastructure in Arabidopsis. – Acta Soc. Bot. Pol. 84: 59-70, 2015. 10.5586/asbp.2015.001 DOI

Bradley R.L., Long K.M., Frasch W.D.: The involvement of photosystem II-generated H2O2 in photoinhibition. – FEBS Lett. 286: 209-213, 1991. 10.1016/0014-5793(91)80975-9 PubMed DOI

Butenko Y., Lin A., Naveh L. et al..: Differential roles of the thylakoid lumenal Deg protease homologs in chloroplast proteostasis. – Plant Physiol. 178: 1065-1080, 2018. 10.1104/pp.18.00912 PubMed DOI PMC

Chassin Y., Kapri-Pardes E., Sinvany G. et al..: Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. – Plant Physiol. 130: 857-864, 2002. 10.1104/pp.007922 PubMed DOI PMC

Chen K., Li H., Chen Y. et al..: TaSCL14, a novel wheat (Triticum aestivum L.) GRAS gene, regulates plant growth, photosynthesis, tolerance to photooxidative stress, and senescence. – J. Genet. Genomics 42: 21-32, 2015. 10.1016/j.jgg.2014.11.002 PubMed DOI

Chen S., Han X., Fang J. et al..: Sedum alfredii SaNramp6 metal transporter contributes to cadmium accumulation in transgenic Arabidopsis thaliana. – Sci. Rep.-UK 7: 13318, 2017. 10.1038/s41598-017-13463-4 PubMed DOI PMC

Choudhury N.K., Behera R.K.: Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents. – Photosynthetica 39: 481-488, 2001. 10.1023/A:1015647708360 DOI

Clausen T., Southan C., Ehrmann M.: The HtrA family of proteases: implications for protein composition and cell fate. – Mol. Cell 10: 443-455, 2002. 10.1016/S1097-2765(02)00658-5 PubMed DOI

Couée I., Sulmon C., Gouesbet G., El Amrani A.: Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. – J. Exp. Bot. 57: 449-459, 2006. 10.1093/jxb/erj027 PubMed DOI

Elstner E.F., Heupel A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. – Anal. Biochem. 70: 616-620, 1976. 10.1016/0003-2697(76)90488-7 PubMed DOI

Haußühl K., Andersson B., Adamska I.: A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. – EMBO J. 20: 713-722, 2001. 10.1093/emboj/20.4.713 PubMed DOI PMC

Hein I., Barciszewska-Pacak M., Hrubikova K. et al..: Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. – Plant Physiol. 138: 2155-2164, 2005. 10.1104/pp.105.062810 PubMed DOI PMC

Holzberg S., Brosio P., Gross C., Pogue G.P.: Barley stripe mosaic virus-induced gene silencing in a monocot plant. – Plant J. 30: 315-327, 2002. 10.1046/j.1365-313X.2002.01291.x PubMed DOI

Horton P.: Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. – J. Exp. Bot. 51: 475-485, 2000. 10.1093/jexbot/51.suppl_1.475 PubMed DOI

Huesgen P.F., Schuhmann H., Adamska I.: The family of Deg proteases in cyanobacteria and chloroplasts of higher plants. – Physiol. Plantarum 123: 413-420, 2005. 10.1111/j.1399-3054.2005.00458.x DOI

Junglee S., Urban L., Sallanon H., Lopez-Lauri F.: Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. – Am. J. Anal. Chem. 5: 730-736, 2014. 10.4236/ajac.2014.511081 DOI

Kapri-Pardes E., Naveh L., Adam Z.: The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. – Plant Cell 19: 1039-1047, 2007. 10.1105/tpc.106.046573 PubMed DOI PMC

Kato Y., Sun X., Zhang L., Sakamoto W.: Cooperative D1 degradation in the photosystem II repair mediated by chloroplastic proteases in Arabidopsis. – Plant Physiol. 159: 1428-1439, 2012. 10.1104/pp.112.199042 PubMed DOI PMC

Ledwożyw A., Michalak J., Stepień A., Kądziołka A.: The relationship between plasma triglycerides, cholesterol, total lipids and lipid-peroxidation products during human atherosclerosis. – Clin. Chim. Acta 155: 275-283, 1986. 10.1016/0009-8981(86)90247-0 PubMed DOI

Li H., Tong Y., Li B. et al..: Genetic analysis of tolerance to photo-oxidative stress induced by high light in winter wheat (Triticum aestivum L.). – J. Genet. Genomics 37: 399-412, 2010. 10.1016/S1673-8527(09)60058-8 PubMed DOI

Li H., Zheng Q., Zhang J. et al..: The analysis of determining factors and evaluation of tolerance to photoinhibition in wheat (Triticum aestivum L.). – Photosynthetica 55: 69-76, 2017. 10.1007/s11099-016-0228-4 DOI

Li W.C., Liu Y.N., Liu M.M. et al..: Sugar accumulation is associated with leaf senescence induced by long-term high light in wheat. – Plant Sci. 287: 110169, 2019. 10.1016/j.plantsci.2019.110169 PubMed DOI

Liu Y.N., Xu Q.Z., Li W.C. et al..: Long-term high light stress induces leaf senescence in wheat (Triticum aestivum L.). – Photosynthetica 57: 830-840, 2019. 10.32615/ps.2019.086 DOI

Luciński R., Misztal L., Samardakiewicz S., Jackowski G.: Involvement of Deg5 protease in wounding-related disposal of PsbF apoprotein. – Plant Physiol. Bioch. 49: 311-320, 2011b. 10.1016/j.plaphy.2011.01.001 PubMed DOI

Luciński R., Misztal L., Samardakiewicz S., Jackowski G.: The thylakoid protease Deg2 is involved in stress-related degradation of the photosystem II light-harvesting protein Lhcb6 in Arabidopsis thaliana. – New Phytol. 192: 74-86, 2011a. 10.1111/j.1469-8137.2011.03782.x PubMed DOI

Miyao M.: Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. – Biochemistry 33: 9722-9730, 1994. 10.1021/bi00198a043 PubMed DOI

Pan C., Lu H., Yu J. et al..: Identification of cadmium-responsive Kandelia obovata SOD family genes and response to Cd toxicity. – Environ. Exp. Bot. 162: 230-238, 2019. 10.1016/j.envexpbot.2019.02.018 DOI

Peltier J.-B., Emanuelsson O., Kalume D.E. et al..: Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. – Plant Cell 14: 211-236, 2002. 10.1105/tpc.010304 PubMed DOI PMC

Peskin A.V., Winterbourn C.C.: A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1). – Clin. Chim. Acta 293: 157-166, 2000. 10.1016/S0009-8981(99)00246-6 PubMed DOI

Petty I.T.D., Hunter B.G., Wei N., Jackson A.O.: Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. – Virology 171: 342-349, 1989. 10.1016/0042-6822(89)90601-6 PubMed DOI

Pospíšil P., Yamamoto Y.: Damage to photosystem II by lipid peroxidation products. – BBA-Gen. Subjects 1861: 457-466, 2017. 10.1016/j.bbagen.2016.10.005 PubMed DOI

Schmittgen T.D., Livak K.J.: Analyzing real-time PCR data by the comparative CT method. – Nat. Protoc. 3: 1101-1108, 2008. 10.1038/nprot.2008.73 PubMed DOI

Schubert M., Petersson U.A., Haas B.J. et al..: Proteome map of the chloroplast lumen of Arabidopsis thaliana. – J. Biol. Chem. 277: 8354-8365, 2002. 10.1074/jbc.M108575200 PubMed DOI

Schuhmann H., Adamska I.: Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. – Physiol. Plantarum 145: 224-234, 2012. 10.1111/j.1399-3054.2011.01533.x PubMed DOI

Schuhmann H., Mogg U., Adamska I.: A new principle of oligomerization of plant DEG7 protease based on interactions of degenerated protease domains. – Biochem. J. 435: 167-174, 2011. 10.1042/BJ20101613 PubMed DOI PMC

Scofield S.R., Huang L., Brandt A.S., Gill B.S.: Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. – Plant Physiol. 138: 2165-2173, 2005. 10.1104/pp.105.061861 PubMed DOI PMC

Sima Y.-H., Yao J.-M., Hou Y.-S. et al..: Variations of hydrogen peroxide and catalase expression in Bombyx eggs during diapause initiation and termination. – Arch. Insect Biochem. Physiol. 77: 72-80, 2011. 10.1002/arch.20422 PubMed DOI

Sinvany-Villalobo G., Davydov O., Ben-Ari G. et al..: Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. – Plant Physiol. 135: 1336-1345, 2004. 10.1104/pp.104.043299 PubMed DOI PMC

Stevens R., Buret M., Garchery C. et al..: Technique for rapid, small-scale analysis of vitamin C levels in fruit and application to a tomato mutant collection. – J. Agr. Food Chem. 54: 6159-6165, 2006. 10.1021/jf061241e PubMed DOI

Stirbet A., Lazár D., Kromdijk J., Govindjee: Chl a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? – Photosynthetica 56: 86-104, 2018. 10.1007/s11099-018-0770-3 DOI

Su T., Wang P., Li H. et al..: The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome-derived signaling in plant development. – J. Integr. Plant Biol. 60: 591-607, 2018. 10.1111/jipb.12649 PubMed DOI

Sulmon C., Gouesbet G., Coueé I., El Amrani A.: Sugar induced tolerance to atrazine in Arabidopsis seedlings: interacting effects of atrazine and soluble sugars on psbA mRNA and D1 protein levels. – Plant Sci. 167: 913-923, 2004. 10.1016/j.plantsci.2004.05.036 DOI

Sun X.W., Fu T.J., Chen N. et al..: The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. – Plant Physiol. 152: 1263-1273, 2010. 10.1104/pp.109.150722 PubMed DOI PMC

Sun X.W., Peng L.W., Guo J.K. et al..: Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. – Plant Cell 19: 1347-1361, 2007a. 10.1105/tpc.106.049510 PubMed DOI PMC

Sun X.W., Wang L.Y., Zhang L.X.: Involvement of Deg5 and Deg8 proteases in the turnover of the photosystem II reaction center D1 protein under heat stress in Arabidopsis thaliana. – Chin. Sci. Bull. 52: 1742-1745, 2007b. 10.1007/s11434-007-0275-0 DOI

Tikkanen M., Mekala N.R., Aro E.-M.: Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. – BBA-Bioenergetics 1837: 210-215, 2014. 10.1016/j.bbabio.2013.10.001 PubMed DOI

Traverso N., Menini S., Maineri E.P. et al..: Malondialdehyde, a lipoperoxidation-derived aldehyde, can bring about secondary oxidative damage to proteins. – J. Gerontol. A 59: B890-895, 2004. 10.1093/gerona/59.9.B890 PubMed DOI

Uauy C., Distelfeld A., Fahima T. et al..: A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. – Science 314: 1298-1301, 2006. 10.1126/science.1133649 PubMed DOI PMC

Ullah S., Kolo Z., Egbichi I. et al..: Nitric oxide influences glycine betaine content and ascorbate peroxidase activity in maize. – S. Afr. J. Bot. 105: 218-225, 2016. 10.1016/j.sajb.2016.04.003 DOI

Wang L., Wang Y., Wang X. et al..: Regulation of POD activity by pelargonidin during vegetative growth in radish (Raphanus sativus L.). – Sci. Hortic.-Amsterdam 174: 105-111, 2014. 10.1016/j.scienta.2014.05.014 DOI

Wu K., Li J., Luo J. et al..: Effects of elevated CO2 and endophytic bacterium on photosynthetic characteristics and cadmium accumulation in Sedum alfredii. – Sci. Total Environ. 643: 357-366, 2018. 10.1016/j.scitotenv.2018.06.131 PubMed DOI

Ying Y., Liu F.F., Li G.P. et al..: Silencing of the receptor-like cytoplasmic kinase gene TaRKL1 reduces photosynthetic capacity in wheat. – Photosynthetica 58: 1188-1199, 2020. 10.32615/ps.2020.069 DOI