Abstract
The photosynthetic oxygen evolution rate, Hill reaction activity of seedlings and photosynthetic parameter, Pn–Ci curve and some source-sink metabolism-related enzyme activities, and substance content of flag leaves were measured by using two wheat near isogenic lines with significant differences in the photosynthetic rate of the 154 (high photosynthetic rate) and 212 (low photosynthetic rate) lines as materials. The results showed that the maximal carboxylation efficiency (Vcmax) and Hill reaction activity were higher in line 154 than that of line 212. The Pn in flag leaves of line 154 was significantly higher than that of line 212 during the anthesis to grain-filling stage. Higher leaf sucrose phosphate synthase activity, grain sucrose synthase activity, and grain ADPG pyrophosphorylase activity ensured that the photosynthate of line 154 could be transported to grains and translated into starch in a timely and effective manner, which also contributed to the maintenance of its high photosynthetic rate. Eventually, all of these factors of line 154 resulted in its higher grain yield compared with the low photosynthetic rate of line 212.
Similar content being viewed by others
Abbreviations
- AGPase:
-
Adenosine diphosphate glucose pyrophosphorylase
- Ci:
-
Intercellular CO2 concentration
- Gs:
-
Stomatal conductance
- Ls:
-
Stomatal limitation value
- NILs:
-
Near isogenic lines
- Pn:
-
Net photosynthetic rate
- SPS:
-
Sucrose phosphate synthase
- SS:
-
Sucrose synthase
- Vcmax:
-
Maximal carboxylation efficiency
References
Araus JL, Ferrio JP, Buxo R, Voltas J (2007) The historical perspective of dryland agriculture: lessons learned from 10,000 years of wheat cultivation. J Exp Bot 58:131–145
Araus JL, Slafer GA, Royo C, Serret MD (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 7:377–412
Awika JM (2011) Major cereal grains production and use around the world. In advances in cereal science: implications to food processing and health promotion., ACS symposium seriesAmerican Chemical Society, Washington DC, pp 1–13
Ballicora MA, Iglesias AA, Preiss J (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth Res 79:1–24
Baroja-Fernández E, Muñoz FJ, Montero M, Etxeberria E, Sesma MT, Ovecka M, Pozueta-Romero J (2009) Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol 50:1651–1662
Bhullar SS, Jenner CF (1985) Differential responses to high temperatures of starch and nitrogen accumulation in the grain of four cultivars of wheat. Funct Plant Biol 12:363–375
Blum A (1990) Variation among wheat cultivars in the response of leaf gas exchange to light. J Agric Sci 115:305–311
Borrás L, Slafer GA, Otegui ME (2004) Seed dry weight response to source-sink manipulations in wheat, maize and soy-bean: a quantitative reappraisal. Field Crops Res 86:131–146
Braun HJ, Atlin G, Payne T (2010) Multi-location testing as a tool to identify plant response to global climate change. Climate change and crop production. CABI Publishers, Wallingford, pp 115–138
Champigny ML (1995) Integration of photosynthetic carbon and nitrogen metabolism in higher plants. Photosynth Res 46:117–127
Cheng JF, Ma WM, Chen GY, Hu MJ, Shen YG, Li ZS, Dong YP, Li B, Li HW (2009) Dynamic changes of photosynthetic characteristics in Xiaoyan 54, Jing 411, and the stable selected superior strains of their hybrid progenies. Acta Agronomica Sinica 35:1051–1058
Conway G, Toenniessen G (1999) Feeding the world in the twenty-first century. Nature 402:C55–C58
Dale EMD, Housley TL (1986) Sucrose synthase activity in developing wheat endosperms differing in maximum weight. Plant Physiol 82:7–10
Delmer DP, Haigler CH (2002) The regulation of metabolic flux to cellulose, a major sink for carbon in plants. Metab Eng 4:22–28
Dixon JM (2009) Wheat facts and futures 2009. CIMMYT, Mexico City
Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13
Eli Zamski, Schaffer AA (1996) Photoassimilate distribution in plants and crops: source-sink relationships. Marcel Dekker, New York
Evans LT (1993) Crop evolution, adaptation and yield. Cambridge University Press, New York
Evans LT (1997) Adapting and improving crops: the endless task. Philosophical transactions of the Royal Society of London. Ser B: Biol Sci 352:901–906
Evans JR (2013) Improving photosynthesis. Plant Physiol 162:1780–1793
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Fischer RA, Edmeades GO (2010) Breeding and cereal yield progress. Crop Sci 50:S85–S98
Fischer RA, Rees D, Sayre KD, Lu ZM, Condon AG, Saavedra AL (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci 38:1467–1475
Hawkesford MJ, Araus JL, Park R, Calderini D, Miralles D, Shen T, Zhang JP, Parry MAJ (2013) Prospects of doubling global wheat yields. Food Energy Secur 2:34–48
He ZH, Xia XC, Chen XM, Zhuang QS (2011) Progress of wheat breeding in china and the future perspective. Acta Agronomica Sinica 37:202–215
Huang J, Pray C, Rozelle S (2002) Enhancing the crops to feed the poor. Nature 418:678–684
Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Ann Rev Plant Biol 47:431–444
Hurkman WJ, McCue KF, Altenbach SB, Korn A, Tanaka CK, Kothari KM, Johnson EL, Bechtel DB, Wilson JD, Anderson OD (2003) Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Sci 164:873–881
Jiang D, Yu ZW, Li YG, Yu SL (2002a) Dynamic changes of enzyme activities involving in starch synthesis in superior and inferior grains of high-yield winter wheat. Scientia Agricultura Sinica 35:378–383
Jiang D, Yu ZW, Li YG, Yu SL (2002b) Effects of different nitrogen application levels on changes of sucrose content in leaf, culm, grain and photosynthate distribution and grain starch accumulation of winter wheat. Scientia Agricultura Sinica 35:157–162
Jiang H, Wang HW, Su JH, Shi XB, Shen YG, Li ZS, Wei QK, Li B, Li M, Zhang JJ (2002c) Photosynthesis in offspring of hybridization between two wheat cultivars. Acta Agronomica Sinica 28:451–454
Keeling PL, Wood JR, Tyson RH, Bridges IG (1988) Starch biosynthesis in developing wheat grain. Plant Physiol 87:311–319
Khush G (2003) Productivity improvements in rice. Nutr Rev 61:S114–S116
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Ann Rev Plant Biol 55:341–372
Lbraheem O, Hove RM, Bradley G (2008) Sucrose assimilation and the role of sucrose transporters in plant wound response. Afr J Biotechnol 7:4850–4855
Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochimica et Biophysica Acta (BBA)-Biomembranes 1465:246–262
Li X, Wang C (2013) Physiological and metabolic enzymes activity changes in transgenic rice plants with increased phosphoenolpyruvate carboxylase activity during the flowering stage. Acta Physiologiae Plantarum 35:1503–1512
Li YG, Yu ZW, Jiang D, Yu SL (2001) Studies on the dynamic changes of the synthesis of sucrose in the flag leaf and starch in the grain and related enzymes of high-yielding wheat. Acta Agronomica Sinica 27:658–664
Li N, Zhang S, Zhao Y, Li B, Zhang J (2011) Over-expression of AGPase genes enhances seed weight and starch content in transgenic maize. Planta 233:241–250
Liu HQ, Jiang GM, Zhang QD, Sun JZ (2002) Changes of gas exchanges in leaves of different cultivars of winter wheat released in different years. Acta Botanica Sinica 44:913–919
Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improved photosynthesis increase crop yields? Plant, Cell Environ 29:315–330
Lu HQ, Shen FF, Liu LX, Su WF (2005) Recent advances in study on plant sucrose synthase. Chin Agric Sci Bull 21:34–37
Ludewig F, Flügge UI (2013) Role of metabolite transporters in source-sink carbon allocation. Front Plant Sci 4:231
Miralles DJ, Slafer GA (2007) Sink limitations to yield in wheat: how could it be reduced? J Agric Sci, Cambridge 145:139–150
Moll RH, Jackson WA, Mikkelsen RL (1994) Recurrent selection for maize grain yield: dry matter and nitrogen accumulation and partitioning changes. Crop Sci 34:874–881
Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytol 18:532–552
Nakamura Yasunori, Yuki Kazuhiro, Park Shin-Young, Ohya Toshihide (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30:833–839
Okita TW (1992) Is there an alternative pathway for starch synthesis? Plant Physiol 100:560–564
Pan QM, Yu ZW, Wang YF, Yu SL (2002) Effects of nitrogen applying stage on both sucrose synthesis in flag leaves and cleavage in grains of wheat. Scientia Agricultura Sinica 35:771–776
Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Furbank RT (2010) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J Exp Bot 62:453–467
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547
Preiss J, Sivak M (1996) Starch synthesis in sinks and sources. In: Photoassimilate Distribution in Plants and Crops, E Zamski (ed), Source-Sink Relationships, Marcel Dekker, New York, NY, USA, pp 139–168
Preiss J, Ball K, Smith-White B (1988) Biosynthesis of starch and its regulation. Biochem Plants 14:181–254
Raines CA (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol 155:36–42
Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MAJ, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60:1899–1918
Reynolds M, Bonnett D, Chapman SC, Furbank RT, Manes Y, Mather DE, Parry MAJ (2011) Raising yield potential of wheat I. Overview of a consortium approach and breeding strategies. J Exp Bot 62:439–453
Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G (2012) Achieving yield gains in wheat. Plant, Cell Environ 35:1799–1823
Rosegrant MW, Agcaoili M (2010) Global food demand, supply, and price prospects to 2010. International Food Policy Research Institute, Washington, DC
Sakamoto T, Matsuoka M (2004) Generating high-yielding varieties by genetic manipulation of plant architecture. Curr Opin Biotechnol 15:144–147
Sakulsingharoj C, Choi SB, Hwang SK, Edwards GE, Bork J, Meyer CR, Okita TW (2004) Engineering starch biosynthesis for increasing rice seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase. Plant Sci 167:1323–1333
Sayre KD, Rajaram S, Fischer RA (1997) Yield potential progress in short bread wheats in northwest Mexico. Crop Sci 37:36–42
Schaffer AA, Petreikov M (1997) Sucrose-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113:739–746
Shearman VJ, Sylvester-Bradley R, Scott RK, Foulkes MJ (2005) Physiological processes associated with wheat yield progress in the UK. Crop Sci 45:175–185
Sheehy JE, Ferrer AB, Mitchell PL, Elmido-Mabilangan A, Pablico P, Dionora MJA (2007) How the rice crop works and why it needs a new engine. In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting new pathways to C4 rice. International Rice Research Institute, Los Baños, pp 3–26
Shewry PR (2009) Wheat. J Exp Bot 60:1537–1553
Sinclair TR, Purcell LC, Sneller CH (2004) Crop transformation and the challenge to increase yield potential. Trends Plant Sci 9:70–75
Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ (2002) Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Nat Acad Sci 99:1724–1729
Smidansky ED, Martin JM, Hannah CL, Fischer AM, Giroux MJ (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216:656–664
Smidansky ED, Meyer FD, Blakeslee B, Weglarz TE, Greene TW, Giroux MJ (2007) Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism. Planta 225:965–976
Stitt M (1989) Control analysis of photosynthetic sucrose synthesis: assignment of elasticity coefficients and flux-control coefficients to the cytosolic fructose-1, 6-bisphosphatase and sucrose phosphate synthase. Philos Trans Royal Society of London B: Biol Sci 323:327–338
Thévenot C, Simond-Côte E, Reyss A, Manicacci D, Trouverie J, Le Guilloux M, Prioul JL (2005) QTLs for enzyme activities and soluble carbohydrates involved in starch accumulation during grain filling in maize. J Exp Bot 56:945–958
Tuncel A, Okita TW (2013) Improving starch yield in cereals by over-expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Sci 211:52–60
Turgeon R (1989) The sink-source transition in leaves. Ann Rev Plant Physiol Plant Mol Biol 40:119–138
Van Camp W (2005) Yield enhancement genes: seeds for growth. Curr Opin Biotechnol 16:147–153
Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387
Wang ZL, He MR (1999) Effects of source sink manipulation on production and distribution of photosynthate after flowering in irrigated and rainfed wheat. Acta Agronomica Sinica 25:162–168
Wang F, Sanz A, Brenner ML, Smith AG (1993) Sucrose synthease, starch accumulation, and tomato fruit sink strength. Plant Physiol 101:321–327
Wang AY, Kao MH, Yang WH, Sayion Yiyang, Liu LF, Lee PD, Su JC (1999) Differentially and developmentally regulated expression of three rice sucrose synthase genes. Plant Cell Physiol 40:800–807
Wang L, Cui N, Zhang KY, Fan HY, Li TL (2013) Research Advance of Sucrose Phosphate Synthase (SPS) in Higher Plant. Intern J Agric Biol 15:1221–1226
Winder TL, Sun J, Okita TW, Edwards GE (1998) Evidence for the occurrence of feedback inhibition of photosynthesis in rice. Plant Cell Physiol 39:813–820
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19:31–67
Worrell AC, Bruneau JM, Summerfelt K, Boersig M, Voelker TA (1991) Expression of a maize sucrose phosphate synthase in tomato alters leaf carbonhydrate partitioning. Plant Cell 3:1121–1130
Xiong FS, Gao YZ, Zhan YC (1994) Relationship between leaf sucrose and starch content and their degradative enzymes activities in crop plants. Acta Agronomica Sinica 20:52–58
Xu DQ (1999) Photosynthetic rate, photosynthetic efficiency and crop yield. Bull Biol 34:8–10
Yang JC, Zhang JH, Wang ZQ, Xu GW, Zhu QS (2004) Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiol 135:1621–1629
Yang XH, Chen XY, Ge QY, Li B, Tong YP, Zhang AM, Li ZS, Kuang TY, Lu CM (2006) Tolerance of photosynthesis to photoinhibition, high temperature and drought stress in flag leaves of wheat: a comparison between a hybridization line and its parents grown under field conditions. Plant Sci 171:389–397
Yang XH, Chen XY, Ge QY, Li B, Tong YP, Zhang AM, Li ZS, Kuang TY, Lu CM (2007) Characterization of photosynthesis of flag leaves in wheat hybrid and its parents grown under field conditions. J Plant Physiol 164:318–326
Ye JY, Qian YQ (1985) Detection of Hill reaction with spectrophotometer. In: Xue YL, Xia ZA (eds) Plant physiology experiment handbook. Shanghai Science and Technology Press, Shanghai, pp 104–107
Zhang QD, Jiang GM, Zhu XG, Wang Q, Lu CM, Bai KZ, Kuang TY (2001) Photosynthetic capability of 12 genotypes of Triticum aestivum. Acta Phytoecologica Sinica 25:532–536
Zhao XX, Ma QQ, Liang C, Fang Y, Wang YQ, Wang W (2007) Effect of glycinebetaine on function of thylakoid membranes in wheat flag leaves under drought stress. Biol Plant 51:584–588
Zheng TC, Zhang XK, Yin GH, Wang LN, Han YL, Chen L, He ZH (2011) Genetic gains in grain yield, net photosynthesis and stomatal conductance achieved in Henan Province of China between 1981 and 2008. Field Crops Res 122:225–233
Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159
Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Ann Rev Plant Biol 61:235–261
Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang XH, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546
Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107
Acknowledgments
This work was supported by the National Natural Sciences Foundation of China (31271634), the National High Technology Research and Development Program of China (2012AA10A309), and the State Key Basic Research and Development Plan of China (2015CB150105).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, B., Ma, M., Lu, H. et al. Photosynthesis, sucrose metabolism, and starch accumulation in two NILs of winter wheat. Photosynth Res 126, 363–373 (2015). https://doi.org/10.1007/s11120-015-0126-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-015-0126-9