Photosynthetica 2023, 61(1):97-107 | DOI: 10.32615/ps.2023.008

Downregulated expression of TaDeg7 inhibits photosynthetic activity in bread wheat (Triticum aestivum L.)

F.F. LIU1, 2, G.P. LI1, H.W. LI2
1 College of Life Sciences, Huaibei Normal University, 235000 Huaibei, China
2 State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 100101 Beijing, China

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.

Additional key words: Deg7 protease; high light; photosynthetic efficiency; virus-induced gene silencing; wheat.

Received: January 5, 2023; Revised: March 7, 2023; Accepted: March 14, 2023; Prepublished online: March 30, 2023; Published: April 13, 2023  Show citation

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LIU, F.F., LI, G.P., & LI, H.W. (2023). Downregulated expression of TaDeg7 inhibits photosynthetic activity in bread wheat (Triticum aestivum L.). Photosynthetica, 61(1), 97-107. doi: 10.32615/ps.2023.008
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    References

    1. Adir N., Zer H., Shochat S., Ohad I.: Photoinhibition - a historical perspective. - Photosynth. Res. 76: 343-370, 2003. Go to original source...
    2. Arnon D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
    3. Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - BBA-Bioenergetics 1143: 113-134,1993. Go to original source...
    4. 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. Go to original source...
    5. Bradley R.L., Long K.M., Frasch W.D.: The involvement of photosystem II-generated H2O2 in photoinhibition. - FEBS Lett. 286: 209-213, 1991. Go to original source...
    6. 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. Go to original source...
    7. 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. Go to original source...
    8. 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. Go to original source...
    9. 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. Go to original source...
    10. Choudhury N.K., Behera R.K.: Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents. - Photosynthetica 39: 481-488, 2001. Go to original source...
    11. Clausen T., Southan C., Ehrmann M.: The HtrA family of proteases: implications for protein composition and cell fate. - Mol. Cell 10: 443-455, 2002. Go to original source...
    12. 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. Go to original source...
    13. Elstner E.F., Heupel A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976. Go to original source...
    14. 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.
    15. 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. Go to original source...
    16. 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. Go to original source...
    17. 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. Go to original source...
    18. 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. Go to original source...
    19. 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. Go to original source...
    20. 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. Go to original source...
    21. 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. Go to original source...
    22. Ledwożyw A., Michalak J., Stepień A., Ka̧dziołka A.: The relationship between plasma triglycerides, cholesterol, total lipids and lipid-peroxidation products during human atherosclerosis. - Clin. Chim. Acta 155: 275-283, 1986. Go to original source...
    23. 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. Go to original source...
    24. 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. Go to original source...
    25. 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. Go to original source...
    26. 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. Go to original source...
    27. 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. Go to original source...
    28. 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. Go to original source...
    29. 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. Go to original source...
    30. 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. Go to original source...
    31. 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. Go to original source...
    32. 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. Go to original source...
    33. 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. Go to original source...
    34. Pospíąil P., Yamamoto Y.: Damage to photosystem II by lipid peroxidation products. - BBA-Gen. Subjects 1861: 457-466, 2017. Go to original source...
    35. Schmittgen T.D., Livak K.J.: Analyzing real-time PCR data by the comparative CT method. - Nat. Protoc. 3: 1101-1108, 2008. Go to original source...
    36. 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. Go to original source...
    37. 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. Go to original source...
    38. 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. Go to original source...
    39. 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. Go to original source...
    40. 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. Go to original source...
    41. 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. Go to original source...
    42. 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. Go to original source...
    43. 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. Go to original source...
    44. 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. Go to original source...
    45. 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. Go to original source...
    46. 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. Go to original source...
    47. 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. Go to original source...
    48. 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. Go to original source...
    49. 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. Go to original source...
    50. 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. Go to original source...
    51. 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. Go to original source...
    52. 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. Go to original source...
    53. 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. Go to original source...
    54. 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. Go to original source...
    55. 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. Go to original source...

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