Abstract
As the last step of leaf development, premature senescence often causes the damage of photosynthetic apparatus and the reduction of active photosynthesis, which leads to a decrease in crop yield. In this study, we investigated the early response of rice NG46 leaves to senescence by following changes in physiological attributes and thylakoid membrane proteins. We found that photosynthetic pigment contents, net photosynthetic rate (PN), stomatal conductance (gs) and transpiration rate (E) decreased significantly, while the contents of superoxide anion (O2·−), malondialdehyde concentration (MDA) and the antioxidant enzyme activities were substantially increased. Analysis of OJIP transients and parameters showed that part of photosystem II (PSII) reaction center (RC) was damaged and electron transport chain was impaired. Blue native page investigations revealed that the amount of supercomplexes increased at the filling stage, while a significant decrease in PSII monomer and cytochrome b6/f (Cyt b6/f) complex was observed. Further analysis of the thylakoid protein complex by 2-D BN/SDS-PAGE showed that the differential proteins were involved in light harvesting, stability and function of photosystems, electron transport, CO2 assimilation rate, and breakdown and repair of thylakoid membranes. Our results suggest that PSII and Cyt b6/f of rice NG46 are extremely susceptible to senescence, which affects the stability of the photosynthetic apparatus and exhibits a low photosynthetic capacity.
Similar content being viewed by others
References
Andaluz S, López-Millán AF, De las Rivas J, Aro EM, Abadía J, Abadía A (2006) Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89:141–155
Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199
Chen S, Cheng L (2009) Photosystem 2 is more tolerant to high temperature in apple (Malus domestica Borkh.) leaves than in fruit peel. Photosynthetica 47:112–120
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Meth Enzymol 186(474):421–431
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620
Erickson JM, Rahire M, Malnoë P, Girard-Bascou J, Pierre Y, Bennoun P, Rochaix JD (1986) Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J 5:1745–1754
Farquhar DG, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–355
Fazeli F, Ghorbanli M, Niknam V (2007) Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars. Biol Plantarum 51:98–103
Fischer AM (2012) The complex regulation of senescence. Crit Rev Plant Sci 31:124–147
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100
Gan S, Amasino RM (1997) Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiol 113:313–319
García-Cerdán JG, Kovács L, Tóth T, Kereïche S, Aseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J 65:14
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gray JC (1996) Biogenesis of chloroplasts in higher plants. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. Bios Scientific Publishers, Oxford, UK, pp 441–458
Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:685–714
Guiamet JJ, Tyystjärvi E, Tyystjärvi T, John I, Kairavuo M, Pichersky P, Noodén LD (2002) Photoinhibition and loss of photosystem II reaction center proteins during senescence of soybean leaves. Enhancement of photoinhibition by the “stay-green” mutation cytG. Physiol Plant 115:468–478
Haider I, Andreo-Jimenez B, Bruno M, Bimbo A, Floková K, Abuauf H, Otang-Ntui V, Guo X, Charnikhova T, Al-Babili S (2018) The interaction of strigolactones with abscisic acid during the drought response in rice. J Exp Bot 69:2403–2414
Humbeck K, Quast S, Krupinska K (1996) Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant Cell Environ 19:337–344
Järvi S, Suorsa M, Tadini L, Ivanauskaite A, Rantala S, Allahverdiyeva Y, Leister D, Aro EM (2016) Thylakoid-bound FtsH proteins facilitate proper biosynthesis of photosystem I. Plant Physiol 171:1333–1343
Jensen PE, Knoetzel J, Scheller HV (2001) The role of PSI-G and PSI-K of higher plants in the interaction between light harvesting complex I and the photosystem I reaction center core. Sci Access 3:117–120
Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh K, Tambussi E, Yanniccari M, Cetner MD, Samboraka IA, Stribet A, Olsovska K, Kunderlikova K, Shelonzek H, Rusinowski S, Baba W (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:67–68
Krieger-Liszkay A, Krupinska K, Shimakawa G (2019) The impact of photosynthesis on initiation of leaf senescence. Physiol Plant 166:148–164
Krupinska K, Mulisch M, Hollmann J, Tokarz K, Zschiesche W, Kage H, Humbeck K, Bilger W (2012) An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiol Plant 144:189–200
Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014
Lee RH, Hsu JH, Huang HJ, Lo SF, Chen SC (2009) Alkaline α-galactosidase degrades thylakoid membranes in the chloroplast during leaf senescence in rice. New Phytol 184:596–606
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic. Methods Enzymol 148(511):350–382
Li J, Pandeya D, Nath K, Zulfugarov IS, Yoo SC, Zhang H, Yoo JH, Cho SH, Koh HJ, Kim DS, Seo HS, Kang BC, Lee CH, Paek NC (2010) ZEBRA-NECROSIS, a thylakoid-bound protein, is critical for the photoprotection of developing chloroplasts during early leaf development. Plant J 62:713–725
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Bio 58:115–136
Lu Q, Lu C, Zhang J, Kuang T (2002) Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of field-grown wheat plants. J Plant Physiol 159:1173–1178
Lu QT, Wen XG, Lu CM, Zhang QD, Kuang TY (2003) Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants. Plant Physiol Biochem 41:749–754
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Morita R, Sato Y, Masuda Y, Nishimura M, Kusaba M (2009) Defect in non-yellow coloring 3, an α/β hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J 59:940–952
Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2010) Functional dissection of two Arabidopsis PsbO proteins PsbO1 and PsbO2. FEBS J 272:2165–2175
Oukarroum A, Schansker G, Strasser RJ (2010) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant 137:188–199
Pintó-Marijuan M, Munné-Bosch S (2014) Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. J Exp Bot 65:3845–3857
Prochazkova D, Sairam RK, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Sci 161:765–771
Reynolds MP, Delgado MI, Gutiérrez-Rodrýguez M, Larqué-Saavedra A (2013) Photosynthesis of wheat in a warm, irrigated environment. I: genetic diversity and crop productivity. Field Crop Res 66:37–50
Roose JL, Wegener KM, Pakrasi HB (2012) The extrinsic proteins of photosystem II. Biochim Biophys Acta 1817:121–124
Sairam RK, Singh DV, Srivastava GC (2003) Changes in activities of antioxidant enzymes in sunflower leaves of different ages. Biol Plantarum 47:61–66
Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andrès CB, Kessler F, Hörtensteiner S, Paek NC (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in ArabidopsisCW. Plant Cell 24:507–518
Schansker G, Toth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261
Schägger H, Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 99:223–231
Schöttler MA, Flügel C, Thiele W, Bock R, Bock R (2007) Knockout of the plastid-encoded PetL subunit results in reduced stability and accelerated leaf age-dependent loss of the cytochrome b6f complex. J Biol Chem 282:976–985
Schöttler MA, Thiele W, Belkius K, Bergner SV, Flügel C, Wittenberg G, Agrawal S, Stegemann S, Ruf S, Bock R (2017) The plastid-encoded PsaI subunit stabilizes photosystem I during leaf senescence in tobacco. J Exp Bot 68:1137–1155
Sinvany-Villalobo G, Davydov O, Ben-Ari G, Zaltsman A, Raskind A, Adam Z (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol 135:1336–1345
Staehelin LA, Arntzen CJ (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 5:1327–1337
Stefanov M, Yotsova E, Markovska Y, Apostolova EL (2018) Effect of high light intensity on the photosynthetic apparatus of two hybrid lines of Paulownia grown on soils with different salinity. Photosynthetica 56:832–840
Strasser RJ, Govindjee (1992) On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. Photosynth Res 1:29–32
Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326
Sobhanian H, Aghaei K, Komatsu S (2011) Changes in the plant proteome resulting form salt stress: toward the creation of salt-tolerant crops? J Proteomics 74:1323–1337
Varotto C, Pesaresi P, Meurer J, Oelmüller R, Steiner-Lange S, Salamini F, Leister D (2000) Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J 22:115–124
Wang YW, Jiang DX, Hou JJ, Chen GX (2019) Physiological characterization and thylakoid ultrastructure analysis in super high-yield hybrid rice leaves under drought stress. Photosynthetica 57:890–896
Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106
Zhang CJ, Chu HJ, Chen GX, Shi DW, Zuo M, Wang J, Lu CG, Wang P, Chen L (2007) Photosynthetic and biochemical activities in flag leaves of a newly developed super high-yield hybrid rice (Oryza sativa) and its parents during the reproductive stage. J Plant Res 120:209–217
Zhang AH, Lu QT, Yin Y, Ding SH, Wen XG, Lu CM (2010) Comparative proteomic analysis provides new insights into the regulation of carbon metabolism during leaf senescence of rice grown under field conditions. J Plant Physiol 167:1380–1389
Zhao H, Dai T, Jing Q, Jiang D, Cao W (2007) Leaf senescence and grain filling affected by post-anthesis high temperatures in two different wheat cultivars. J Plant Growth Regul 51:149–158
Acknowledgments
This work was funded by the Jiangsu Agriculture Science and Technology Innovation Found (CX173022; CX181001), Natural Science Foundation of Jiangsu province of China (BK20171034).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by G. Bartosz.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiang, D., Zeng, Y., Almakas, A. et al. Physiological features and thylakoid membrane proteomic analysis of rice NG46 during natural leaf senescence. Acta Physiol Plant 43, 19 (2021). https://doi.org/10.1007/s11738-020-03193-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-020-03193-y