Abstract
Understanding distribution and transport of carbon assimilates and photosynthesis contribution to grain yield in wheat spike is important in assessing the photosynthetic process under stress conditions. In this study, photosynthetic characteristics were evaluated in a pot experiment. Transport of spike photosynthates to grain was demonstrated using 14C isotope tracer technique. Yield and key enzyme activities of C3 and C4 pathways were examined after anthesis in wheat cultivars of different drought resistance. The ear net photosynthetic rate, chlorophyll content of the spike bracts (glume, lemma, and palea), and relative water content slightly decreased under water deficit in drought resistant variety Pubing 143 (Pub) during the grain filling stage, whereas all parameters decreased significantly in drought sensitive variety Zhengyin 1 (Zhe). Grain 14C-photosynthate distribution rate fell by 3.8% in Pub and increased by 3.9% in Zhe. After harvest, the water-use efficiency of Zhe dropped by 18.7% under water deficit. Rubisco activity in ear organs declined significantly under water deficit, whereas activity of C4 pathway enzymes was significantly enhanced, especially that of phosphoenolpyruvate carboxylase and NADP-malate dehydrogenase. Water deficit exerted lesser influence on spike photosynthesis in Pub. Ear organs exhibited delayed senescence. Accumulation of photosynthetic carbon assimilates in ear bracts occurred mainly during the early grain filling and photosynthates were transported in the middle of grain filling. C4 pathway enzymes seem to play an important function in ear photosynthesis. We speculate that the high enzyme activity of the C4 pathway and the increased capacity of photosynthetic carbon assimilate transport were the reasons for the drought tolerance characteristics of ears.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Abbreviations
- CA:
-
carbonic anhydrase
- CAM:
-
crassulacean acid metabolism
- Chl:
-
chlorophyll
- DM:
-
dry mass
- E :
-
transpiration rate
- FM:
-
fresh mass
- MDH:
-
malate dehydrogenase
- NAD-ME:
-
NAD-malic enzyme
- NADP-MDH:
-
NADP-malate dehydrogenase
- NADP-ME:
-
NADP-malic enzyme
- OD:
-
optical density
- PEPC:
-
phosphoenolpyruvate carboxylase
- P N :
-
net photosynthetic rate
- PPDK:
-
pyruvate orthophosphate dikinase
- RWC:
-
relative water content
- TM:
-
turgid mass
- WUE:
-
water-use efficiency
References
Abebe T., Melmaiee K., Berg V. et al.: Drought response in the spikes of barley: gene expression in the lemma, palea, awn, and seed. — Funct. Integr. Genomics 10: 191–205, 2010.
Aoyagi K., Bassham J.A.: Pyruvate orthophosphate dikinase in wheat leaves. — Plant Physiol. 73: 853–854, 1983.
Aoyagi K., Bassham J.A.: Pyruvate orthophosphate dikinase of C3 seeds and leaves as compared to the enzyme from maize. — Plant Physiol. 75: 387–392, 1984a.
Aoyagi K., Bassham J.A.: Pyruvate orthophosphate dikinase mRNA organ specificity in wheat and maize. — Plant Physiol. 76: 278–280, 1984b.
Araus J., Brown H., Febrero A. et al.: Ear photosynthesis, carbon isotope discrimination and the contribution of respiratory CO2 to differences in grain mass in durum wheat. — Plant Cell Environ. 16: 383–392, 1993.
Blanke M.M., Ebert G.: Phosphoenolpyruvate carboxylase and carbon economy of apple seedlings. — J. Exp. Bot. 43: 965–968, 1992.
Bort J., Brown R.H., Araus J.L.: Lack of C4 photosynthetic metabolism in ears of C3 cereals. — Plant Cell Environ. 18: 697–702, 1995.
Bort J., Brown R.H., Araus J.L.: Refixation of respiratory CO2 in the ears of C3 cereals. — J. Exp. Bot. 47: 1567–1575, 1996.
Bort J., Febrero T.A.: Role of awns in ear water-use efficiency and grain mass in barley. — Agronomie 14: 133–139, 1994.
Brownell P., Bielig L., Grof C.: Increased carbonic anhydrase activity in leaves of sodium deficient C4 plants. — Aust. J. Plant Physiol. 18: 589–592, 1991.
Camp P.J., Huber S.C., Burke J.J. et al.: Biochemical changes that occur during senescence of wheat leaves: I. Basis for the reduction of photosynthesis. — Plant Physiol. 70: 1641–1646, 1982.
Comstedt D., Boström B., Marshall J.D. et al.: Effects of elevated atmospheric carbon dioxide and temperature on soil respiration in a boreal forest using δ13C as a labelling tool. — Ecosystems 9: 1266–1277, 2007.
Davood E.A., Alireza H.: Rubisco and PEP-carboxylase levels in relation to grain development within a spikelet of wheat. — Adv. Environ. Biol. 5: 1746–1750, 2011.
Ekblad A., Högberg P.: Analysis of δ13C of CO2 distinguishes between microbial respiration of added C4-sucrose and other soil respiration in a C3-ecosystem. — Plant Soil 219: 197–209, 2000.
Gajewska E., Niewiadomska E., Tokarz K. et al.: Nickelinduced changes in carbon metabolism in wheat shoots. — J. Plant Physiol. 170: 369–377, 2013.
González M.C., Echevarría C., Vidal J. et al.: Isolation and characterisation of a wheat phosphoenolpyruvate carboxylase gene. Modelling of the encoded protein. — Plant Sci. 162: 233–238, 2002.
González M.C., Osuna L., Echevarría C. et al.: Expression and localization of phosphoenolpyruvate carboxylase in developing and germinating wheat grains. — Plant Physiol. 116: 1249–1258, 1998.
González M.C., Sanchez-Bragado R., Cejudo F.J.: Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings. — Planta 216: 985–992, 2003.
Hu W., Huang C., Deng X. et al.: TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. — Plant Cell Environ. 8: 1449–1464, 2013.
Inoue T., Inanaga S., Sugimoto Y. et al.: Effect of drought on ear and flag leaf photosynthesis of two wheat cultivars differing in drought resistance. — Photosynthetica 42: 559–565, 2004.
Kong L., Wang F., Feng B. et al.: The structural and photosynthetic characteristics of the exposed peduncle of wheat (Triticum aestivum L.): an important photosynthate source for grain-filling. — BMC Plant Biol. 10: 1–10, 2010.
Kuzyakov Y., Domanski G.: Model for rhizodeposition and CO2 efflux from planted soil and its validation by 14C pulse labelling of ryegrass. — Plant Soil 239: 87–102, 2002.
Li H., Cai J., Jiang D. et al.: Carbohydrates accumulation and remobilization in wheat plants as influenced by combined waterlogging and shading stress during grain filling. — J. Agron. Crop Sci. 199: 38–48, 2013.
Li X., Hou J., Bai K. et al.: Activity and distribution of carbonic anhydrase in leaf and ear parts of wheat (Triticum aestivum L.). — Plant Sci. 166: 627–632, 2004.
Martinez D.E., Luquez V.M., Bartoli C.G. et al.: Persistence of photosynthetic components and photochemical efficiency in ears of water-stressed wheat (Triticum aestivum). — Physiol. Plantarum 119: 519–525, 2003.
Matsuhashi S., Fujimaki S., Uchida H. et al.: A new visualization technique for the study of the accumulation of photoassimilates in wheat grains using 11CO2. — Appl. Radiat. Isotopes 64: 435–440, 2006.
Matsuoka M. Hata S.: Comparative studies of phosphoenolpyruvate carboxylase from C3 and C4 plants. — Plant Physiol. 85: 947–951, 1987.
Maydup M.L., Antonietta M., Guiamet J.J. et al.: The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). — Field Crop. Res. 119: 48–58, 2010.
Maydup M.L., Antonietta M., Guiamet J.J. et al.: The contribution of green parts of the ear to grain filling in old and modern cultivars of bread wheat (Triticum aestivum L.): Evidence for genetic gains over the past century. — Field Crop Res. 134: 208–215, 2012.
Moroney J.V., Husic H.D., Tolbert N.E.: Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. — Plant Physiol. 79: 177–183, 1985.
Nagy Z., Guóth A., Németh E. et al.: Metabolic indicators of drought stress tolerance in wheat: Glutamine synthetase isoenzymes and Rubisco. — Plant Physiol. Biochem. 67: 48–54, 2013.
Nguyen C., Todorovic C., Robin C. et al.: Continuous monitoring of rhizosphere respiration after labelling of plant shoots with 14CO2. — Plant Soil 212: 189–199, 1999.
Ostle N., Ineson P., Benham D. et al.: Carbon assimilation and turnover in grassland vegetation using an in situ13CO2 pulse labelling system. — Rapid Commun. Mass Sp. 14: 1345–1350, 2000.
Osuna L., González M.C., Cejudo F.J. et al.: In vivo and in vitro phosphorylation of the phosphoenolpyruvate carboxylase from wheat seeds during germination. — Plant Physiol. 111: 551–558, 1996.
Pang J., Palta J.A., Rebetzke G.J., Milroy S.P.: Wheat genotypes with high early vigour accumulate more nitrogen and have higher photosynthetic nitrogen use efficiency during early growth. — Funct. Plant Biol, 41: 215–222, 2013.
Ren Y.T., Lv J.Y., Cheng J.: [Effects of water deficit on photosynthetic characteristics, accumulation and transportation of 14C-assimilates of ears in wheat.] — J. Triticeae Crops 32: 683–688, 2012. [In Chinese]
Sanchez-Bragado R., Elazab A., Zhou B. et al.: Contribution of the ear and the flag leaf to grain filling in durum wheat inferred from the carbon isotope signature: genotypic and growing conditions effects. — J. Integr. Plant Biol. 56: 444–454, 2014.
Sánchez-Díaz M., García J., Antolín M. et al.: Effects of soil drought and atmospheric humidity on yield, gas exchange, and stable carbon isotope composition of barley. — Photosynthetica 40: 415–421, 2002.
Sayre R.T, Kennedy R.A., Pringnitz D.J.: Photosynthetic enzyme activities and localization in Mollugo verticillata populations differing in the levels of C3 and C4 cycle operation. — Plant Physiol. 64: 293–299, 1979.
Schwender J., Goffman F., Ohlrogge J.B. et al.: Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. — Nature 432: 779–782, 2004.
Singal H.B., Sheoran I.S., Singh R.: In vitro enzyme activities and products of 14CO2 assimilation in flag leaf and ear parts of wheat (Triticum aestivum L.). — Photosynth. Res. 8: 113–122, 1986.
Steinmeyer F.T., Martin L., Matthew P. R. et al.: Quantifying the relationship between temperature regulation in the ear and floret development stage in wheat (Triticum aestivum L.) under heat and drought stress — Funct. Plant Biol. 40: 700–707, 2013.
Tambussi E.A., Bort J., Guiamet J.J. et al.: The photosynthetic role of ears in C3 cereals: Metabolism, water use efficiency and contribution to grain yield. — Crit. Rev. Plant Sci. 26: 1–16, 2007.
Teare I.D., Peterson C.J.: Surface area of chlorophyll-containing tissue on the inflorescence of Triticum aestivum L. — Crop Sci. 11: 627–628, 1971.
Thornton B., Paterson E., Midwood A.J. et al.: Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labelling. — Physiol. Plantarum 120: 434–441, 2004.
Tsuzuki M., Miyachi S., Edwards G.E.: Localization of carbonic anhydrase in mesophyll cells ofterrestrial C3 plants in relation to CO2 assimilation. — Plant Cell Physiol. 26: 881–891, 1985.
Wang Z.M., Zhang Y.H., Zhang Y.P. et al.: [Review on photosynthetic performance of ear organs in Triticeae crops.] — J. Triticeae Crops 24: 136–139, 2004. [In Chinese]
Wei A.L., Wang Z.M., Zhai Z.X. et al.: [Effect of soil drought on C4 photosynthetic enzyme activities of flag leaf and ear in wheat.] — Sci. Agric. Sin. 36: 508–512, 2003. [In Chinese]
Xue Q., Zhu Z., Musick J.T. et al.: Physiological mechanisms contributing to the increased water-use efficiency in winter wheat under deficit irrigation. — J. Plant Physiol. 163: 154–164, 2006.
Zhang Y.H., Zhou S.L., Huang Q. et al.: Effects of sucrose and ammonium nitrate on phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase activities in wheat ears. — Aust. J. Crop Sci. 6: 822–827, 2012.
Zhang L., Lv J.Y., Jia S.L.: [Photosynthetic characteristics of spike and distribution of 14C-assimilates accumulated before anthesis in wheat under water deficit condition.] — Acta Agron. Sin. 39: 1514–1519, 2013. [In Chinese]
Zhang Y.H., Su D., Zhang S.Q. et al.: [Phosphoenolpyruvate carboxylase activity of flag leaf and ear organs and its relationship with grain mass and protein content in winter wheat under different water treatments.] — J. Triticeae Crops 29: 997–1003, 2009. [In Chinese]
Zhang Y.P., Wang Z.M., Wang P. et al.: [Canopy photosynthetic characteristics of population of winter wheat in water-saving and high-yielding cultivation.] — Sci. Agric. Sin. 36: 1143–1149, 2003. [In Chinese]
Zhang Y.P., Zhang Y.H., Wang Z.M.: [Photosynthetic diurnal variation characteristics of leaf and non-leaf organs in winter wheat under different irrigation regimes.] — Acta Ecol. Sin. 31: 1312–1322, 2011. [In Chinese]
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: This study is supported by projects of the National Natural Science Foundation of China (31271624). We thank Professor Puling Liu for the technical assistance.
This article is published with open access at springerlink.bibliotecabuap.elogim.com
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Jia, S., Lv, J., Jiang, S. et al. Response of wheat ear photosynthesis and photosynthate carbon distribution to water deficit. Photosynthetica 53, 95–109 (2015). https://doi.org/10.1007/s11099-015-0087-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-015-0087-4