水稻耕作栽培合辑Rice Physiology · Biochemistry · Cultivation · Tillage
|Photosynthetic properties of the mid-vein and leaf lamina of field-grown, high-yield hybrid rice during senescence
|GAO Zhi-ping1*, XU Min-li1*, ZHANG Hai-zi1, LÜ Chuan-gen2, CHEN Guo-xiang1
|1 College of Life Sciences, Nanjing Normal University, Nanjing 210023, P.R.China
2 Institute of Food and Crops, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, P.R.China
Abstract Previous studies with rice (Oryza sativa L.) have shown that the different components of the photosynthetic apparatus are not uniformly synthesized or degraded during senescence. However, while most of those studies have focused on the leaf lamina, few have addressed senescence-associated chloroplast function or leaf physiology. Here, we investigated the photosynthetic properties of the mid-vein and leaf lamina in a high-yield hybrid rice cultivar (Liangyoupei 9, LYP9) during the senescence stage. Assimilation and transpiration decreased more slowly in the mid-vein than in the lamina during senescence, suggesting more sustained photosynthesis in the mid-vein, as well as stronger heat dissipation. Two-dimensional gel electrophoresis suggested that photosynthesis and energy metabolism were less affected by senescence in the mid-vein than in the leaf lamina. During late senescence, the excess energy dissipation in the mid-vein through the xanthophyll cycle had a higher active photosynthetic capacity than in the leaf lamina, and we inferred that the mid-vein and leaf lamina of LYP9 rice differed in terms of their maturation. Taken together, these results provide new insights into the underlying mechanisms of senescence of the rice mid-vein and associated physiology.
Received: 02 December 2020
Accepted: 02 March 2021
|Fund: This work was supported by the National Natural Science Foundation of China (32101639), the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD) and the Jiangsu Agriculture Science and Technology Innovation Fund, China (JASTIF, CX181001).
|About author: GAO Zhi-ping, E-mail: firstname.lastname@example.org; XU Min-li, E-mail: email@example.com; Correspondence CHEN Guo-xiang, E-mail: firstname.lastname@example.org
* These authors contributed equally to this study.
Cite this article:
GAO Zhi-ping, XU Min-li, ZHANG Hai-zi, LÜ Chuan-gen, CHEN Guo-xiang.
Photosynthetic properties of the mid-vein and leaf lamina of field-grown, high-yield hybrid rice during senescence. Journal of Integrative Agriculture, 21(7): 1913-1926.
| Apweiler R, Biswas M, Fleischmann W, Kanapin A, Karavidopoulou Y. 2002. Proteome Analysis Database: Online application of InterPro and CluSTr for the functional classification of proteins in whole genomes. Nucleic Acids Research, 29, 44–48.
Arnon D I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24, 1–16.
Aschan G, Pfanz H. 2003. Non-foliar photosynthesis - A strategy of additional carbon acquisition. Flora, 198, 81–97.
Aubry S, Brown N J, Hibberd M J. 2011. The role of proteins in C3 plants prior to their recruitment into the C4 pathway. Journal of Experimental Botany, 62, 3049–3059.
Baek D, Jin Y, Jeong J C, Lee H J, Moon H, Lee J. 2008. Suppression of reactive oxygen species by glyceraldehyde-3-phosphate dehydrogenase. Phytochemistry, 69, 333–338.
Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van-Staveren M, Stiekema W. 1998. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature, 391, 485–488.
Biswal B. 1995. Caroenoid catabolism during leaf senescence and its control by light. Journal of Experimental Botany, 30, 3–13.
Biswal B, Mohapatra P K, Biswal U C, Raval M K. 2012. Leaf senescence and transformation of chloroplasts to gerontoplasts. Photosynthesis, 34, 217–230.
Biswal U C, Prasanna M. 1978. Changes in the ability of photophosphorylation and activities of surface-bound adenosine triphosphatase and ribulose diphosphate carboxylase of chloroplasts isolated from the barley leaves senescing in darkness. Plant Physiology, 44, 127–133.
Brown N J, Palmer B G, Stanley S, Hajaji H, Janacek S H, Astley H M, Parsley K, Kajala K, Quick W P, Trenkamp S, Fernie A R, Maurino V G, Hibberd J M. 2010. C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. Plant Journal, 61, 122–133.
Carpentier S C, Witters E, Laukens K, Deckers P, Swennen R, Panis B. 2005. Preparation of protein extracts from recalcitrant plant tissues: An evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics, 5, 2497–2507.
Casano L M, Zapata J M, Martín M, Sabater B. 2000. Chlororespiration and poising of cyclic electron transport: Plastoquinone as electron transporter between thylakoid nadh dehydrogenase and peroxidase. Journal of Biological Chemistry, 275, 942–948.
Chen K, Hu G Q, Keutgen N, Blanke M, Lenz F. 1997. Effects of CO2 concentration on strawberry. II. Leaf photosynthetic function. Angewandte Botanik, 71, 173–178.
Cheng L, Ma F. 2004. Diurnal operation of the xanthophyll cycle and the antioxidant system in apple peel. Journal of the American Society for Horticultural Science, 129, 313–320.
Choudhury N K, Behera R K. 2001. Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica, 39, 481–488.
Clermont M G. 2003. Book review Chloroplast biogensis: from proplastid to gerontoplast. Photosynthesis Research, 82, 197–198.
Demmig-Adams B, Gilmore A, Adams W. 1996. In vivo functions of carotenoids in higher plants. Faseb Journal, 10, 403–412.
Deoa P M, Biswalb B. 2001. Response of senescing cotyledons of clusterbean to water stress in moderate and low light: possible photoprotective role of β-carotene. Physiologia Plantarum, 112, 47–54.
Dima E, Manetas Y, Psaras G K. 2006. Chlorophyll distribution pattern in inner stem tissues: Evidence from epifluorescence microscopy and reflectance measurements in 20 woody species. Trees, 20, 515–521.
Feller U, Anders I, Mae T. 2008. Rubiscolytics: Fate of Rubisco after its enzymatic function in a cell is terminated. Journal of Experimental Botany, 59, 1615–1624.
Fernie A R, Carrari F, Sweetlove L J. 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology, 7, 254–261.
Fischer A, Feller U. 1994. Senescence and protein degradation in leaf segments of young winter wheat: Influence of leaf age. Journal of Experimental Botany, 45, 103–109.
Gao Z P, Shen W J, Chen G X. 2018. Uncovering C4-like photosynthesis in C3 vascular cells. Journal of Experimental Botany, 69, 3531–3540.
Ginsburg S, Schellenberg M, Matile P. 1994. Cleavage of chlorophyll-porphyrin: Requirement for reduced ferredoxin and oxygen. Plant Physiology, 105, 545–554.
Grover A. 1993. How do senescing leaves lose photosynthetic activity? Science, 64, 226–233.
Guéra A, Sabater B. 2002. Changes in the protein and activity levels of the plastid, NADH-plastoquinone-oxidoreductase complex during fruit development. Plant Physiology and Biochemistry, 40, 423–429.
Guha A, Sengupta D, Reddy A R. 2013. Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. Journal of Photochemistry and Photobiology (B: Biology), 119, 71–83.
Harding S A, Guikema J A, Paulsen G M. 1990. Photosynthetic decline from high temperature stress during maturation of wheat. Plant Physiology, 92, 648–653.
Hebeler R, Oeljeklaus S, Reidegeld K A, Eisenacher M, Stephan C, Sitek B, Stuhler K, Meyer H E, Sturre M J, Dijkwel P P, Warscheid B. 2008. Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14N/15N labeling and difference gel electrophoresis. Molecular & Cellular Proteomics, 7, 108–120.
Hibberd J M, Covshoff S. 2010. The regulation of gene expression required for C4 photosynthesis. Annual Review of Plant Biology, 61, 181–207.
Hibberd J M, Quick W P. 2002. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature, 415, 451–454.
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 and Environment, 19, 337–344.
Jespersen D, Huang B. 2015. Proteins associated with heat-induced leaf senescence in creeping bentgrass as affected by foliar application of nitrogen, cytokinins, and an ethylene inhibitor. Proteomics, 15, 798–812.
Kalachanis D, Manetas Y. 2010. Analysis of fast chlorophyll fluorescence rise (O-K-J-I-P) curves in green fruits indicates electron flow limitations at the donor side of PSII and the acceptor sides of both photosystems. Physiologia Plantarum, 139, 313–323.
Kato Y, Sakamoto W. 2013. Plastid protein degradation during leaf development and senescence: Role of proteases and chaperones. Advances in Photosynthesis Respiration, 36, 453–477.
Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M, Tanaka A. 2007. Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell, 19, 1362–1375.
Kügler M, Jänsch L, Kruft V, Schmitz U K, Braun H P. 1997. Analysis of the chloroplast protein complexes by blue-native polyacrylamide gel electrophoresis (BN-PAGE). Photosynthesis Research, 53, 35–44.
Li W, Tang X, Xing J, Sheng X, Zhan W. 2014. Proteomic analysis of differentially expressed proteins in Fenneropenaeus chinensis hemocytes upon white spot syndrome virus infection. PLoS ONE, 9, e89962.
Lichtenthaler H, Wellburn A. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591–592.
Lu C M, Lu Q T, Zhang J H, Kuang T Y. 2001. Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field. Journal of Experimental Botany, 52, 1805–1810.
Ma J, Lv C F, Xu M L, Chen G X, Lv C G, Gao Z P. 2016. Photosynthesis performance, antioxidant enzymes, and ultrastructural analyses of rice seedlings under chromium stress. Environmental Science and Pollution Research, 23, 1768–1778.
Manetas Y. 2004. Probing corticular photosynthesis through in vivo chlorophyll fluorescence measurements: Evidence that high internal CO2 levels suppress electron flow and increase the risk of photoinhibition. Physiologia Plantarum, 120, 509–517.
Mohapatra P K, Patro L, Raval M K, Ramaswamy N K, Biswal U C, Biswal B. 2010. Senescence-induced loss in photosynthesis enhances cell wall beta-glucosidase activity. Plant Physiology, 138, 346–355.
Munne-Bosch S, Penuelas J. 2003. Photo- and antioxidative protection during summer leaf senescence in Pistacia lentiscus L. grown under Mediterranean field conditions. Annals of Botany, 9, 385–391.
Nwugo C C, Huerta A J. 2011. The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmium-stress. Journal of Proteome Research, 10, 518–528.
Onda Y, Kobori Y. 2014. Differential activity of rice protein disulfide isomerase family members for disulfide bond formation and reduction. Federation of European Biochemical Societies, 4, 730–734.
Panda D, Sarkar R K. 2013. Natural leaf senescence: probed by chlorophyll fluorescence, CO2, photosynthetic rate and antioxidant enzyme activities during grain filling in different rice cultivars. Physiology and Molecular Biology of Plants, 19, 43–51.
Pavlovič A, Singerová L, Demko V, Hudák J. 2009. Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis. Annals of Botany, 104, 307–314.
Petrie P R, Trought M C T, Howell G S. 2000. Influence of leaf ageing, leaf area and crop load on photosynthesis, stomatal conductance and senescence of grapevine (Vitis vinifera L. cv. Pinot noir) leaves. Vitis, 39, 31–36.
Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M. 2002. Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften, 89, 147–162.
Plaxton W C. 1996. The organization and regulation of plant glycolysis. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 185–214.
Prakash J, Baig M, Mohanty P. 1998. Alterations in electron transport characteristics during senescence of Cucumis cotyledonary leaves. Analysis of the effects of inhibitors. Photosynthetica, 35, 345–352.
Quirino B F, Noh Y S, Himelblau E, Amasino R M. 2000. Molecular aspects of leaf senescence. Trends in Plant Science, 5, 278–282.
Rivelli A R, Loverlli S, Perniola M. 2002. Effects of salinity on gas exchange, water relations and growth of sunflower (Helianthus annuus). Functional Plant Biology, 29, 1405–1415.
Shen W J, Ye L H, Ma J, Yuan Z, Zheng B G, Lv C G, Zhu Z Q, Chen X, Gao Z P, Chen G X. 2016. The existence of C4-bundle-sheath-like photosynthesis in the mid-vein of C3 rice. Rice, 9, 1–14.
Sherman M Y, Sherman M, Gabai V O, O’Callaghan C, Yaglom J. 2007. Molecular chaperones regulate p53 and suppress senescence programs. Febs Letters, 581, 3711–3715.
Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A. 1998. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proceedings of the National Academy of Sciences of the United States of America, 95, 9705–9709.
Silim S, Guy R, Patterson T, Livingston N. 2001. Plasticity in water-use efficiency of Picea sitchensis, P. glauca and their natural hybrids. Oecologia, 128, 317–325.
Sobhanian H, Aghaei K, Komatsu S. 2011. Changes in the plant proteome resulting from salt stress: Toward the creation of salt-tolerant crops? Journal of Proteomics, 74, 1323–1337.
Strasserf R J, Srivastava A, Govindjee. 1995. Polyphasic chlorophyll a, fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology, 61, 32–42.
Timperio A M, Egidi M G, Zolla L. 2008. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). Journal of Proteomics, 71, 391–411.
Vallejos R, Arana J, Ravizzini R. 1983. Changes in activity and structure of the chloroplast proton ATPase induced by illumination of spinach leaves. The Journal of Biological Chemistry, 258, 7317–7321.
Wang F B, Liu J C, Chen M X, Zhou L J, Li Z W, Zhao Q, Pan G, Zaidi S H R, Cheng F M. 2016. Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE, 11, 1–25.
Wang W, Vignani R, Scali M, Cresti M. 2006. A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis, 27, 2782–2786.
Wilson K A, McManus M T, Gordon M E, Jordan T W. 2002. The proteomics of senescence in leaves of white clover, Trifolium repens (L.). Proteomics, 2, 1114–1122.
Wright A H, DeLong J M, Gunawardena A H, Prange R K. 2011. The interrelationship between the lower oxygen limit, chlorophyll fluorescence and the xanthophyll cycle in plants. Photosynthesis Research, 107, 223–235.
Wu L J, Han Z P, Wang S X, Wang X T, Sun A G, Zu X F, Chen Y H. 2013. Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. Journal of Proteomics, 89, 124–140.
Yokota A, Kawasaki S, Iwano M, Nakamura C, Miyake C, Akashi K. 2002. Citrulline and DRIP-1 protein (ArgE homologue) in drought tolerance of wild watermelon. Annals of Botany, 89, 825–832.
Yu G H, Li W, Yuan Z Y, Cui H Y, Lv C G, Gao Z P, Han B, Gong Y Z, Chen G X. 2012. The effects of enhanced UV-B radiation on photosynthetic and biochemical activities in super-high-yield hybrid rice Liangyoupeijiu at the reproductive stage. Photosynthetica, 51, 33–44.
Zhang C J, Chen G X, Gao X X, Chu H J. 2006. Photosynthetic decline in flag leaves of two field-grown spring wheat cultivars with different senescence properties. South African Journal of Botany, 72, 15–23.
Zhu X Y, Chen G C, Zhang C L. 2001. Photosynthetic electron transport, photophosphorylation, and antioxidants in two ecotypes of reed (Phragmites communis Trin.) from different habitats. Photosynthetica, 39, 183–189.
|No Suggested Reading articles found!