Skip to main content
SpringerLink
Log in

Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Assessment of photosynthetic traits and temperature tolerance was performed on field-grown modern genotype (MG), and the local landrace (LR) of wheat (Triticum aestivum L.) as well as the wild relative species (Aegilops cylindrica Host.). The comparison was based on measurements of the gas exchange (A/ci, light and temperature response curves), slow and fast chlorophyll fluorescence kinetics, and some growth and leaf parameters. In MG, we observed the highest CO2 assimilation rate \(\left( {{A_{{\text{C}}{{\text{O}}_2}}}} \right),\) electron transport rate (Jmax) and maximum carboxylation rate \(\left( {{V_{{{\text{C}}_{\hbox{max} }}}}} \right)\). The Aegilops leaves had substantially lower values of all photosynthetic parameters; this fact correlated with its lower biomass production. The mesophyll conductance was almost the same in Aegilops and MG, despite the significant differences in leaf phenotype. In contrary, in LR with a higher dry mass per leaf area, the half mesophyll conductance (gm) values indicated more limited CO2 diffusion. In Aegilops, we found much lower carboxylation capacity; this can be attributed mainly to thin leaves and lower Rubisco activity. The difference in CO2 assimilation rate between MG and others was diminished because of its higher mitochondrial respiration activity indicating more intense metabolism. Assessment of temperature response showed lower temperature optimum and a narrow ecological valence (i.e., the range determining the tolerance limits of a species to an environmental factor) in Aegilops. In addition, analysis of photosynthetic thermostability identified the LR as the most sensitive. Our results support the idea that the selection for high yields was accompanied by the increase of photosynthetic productivity through unintentional improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

\({A_{{\text{C}}{{\text{O}}_2}}}\) :

CO2 assimilation rate

c a :

Reference CO2 concentration

c i :

Intercellular CO2 concentration

F 0 :

Basal fluorescence

F v/F m :

Maximum quantum yield of photosystem II photochemistry

g m :

Mesophyll conductance

J max :

Electron transport rate

LMA:

Dry mass per leaf area

LR:

Local landrace

MG:

Modern genotype

PPFD:

Photosynthetic photon flux density

PSII:

Photosystem II

RH:

Relative air humidity

\(\left( {{V_{{{\text{C}}_{\hbox{max} }}}}} \right)\) :

Maximum carboxylation rate

VPD:

Vapor pressure deficit

WR:

Wild relative

References

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol 165:351–371

    Article  PubMed  Google Scholar 

  • Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OC, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Ra HSY, Zhu XG, Curtis PS, Long SP (2002) A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield. Glob Change Biol 8:695–709

    Article  Google Scholar 

  • Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B 104:1–8

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657(1):23–32

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36:4149–4154

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  CAS  PubMed  Google Scholar 

  • Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ, Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Exp Bot 46:1269–1276

    Article  CAS  Google Scholar 

  • Barbour MM, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant Cell Environ 33:1176–1185

    PubMed  Google Scholar 

  • Bender J, Hertstein U, Black CR (1999) Growth and yield responses of spring wheat to increasing carbon dioxide, ozone and physiological stresses: a statistical analysis ‘ESPACE-wheat’ results. Eur J Agron 10:185–195

    Article  Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24(2):253–259

    Article  CAS  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance: implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borrás L, Slafer GA, Otegui ME (2004) Seed dry weight response to source-sink manipulations in wheat, maize and soybean: a quantitative reappraisal. Field Crop Res 86:131–146

    Article  Google Scholar 

  • Brestic M, Zivcak M (2013) Photosystem II fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer, Heidelberg, pp 87–131

    Chapter  Google Scholar 

  • Brestic M, Zivcak M, Kalaji HM, Allakhverdiev SI, Carpentier R (2012) Photosystem II thermo-stability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105

    Article  CAS  PubMed  Google Scholar 

  • Brestic M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynth Res 130(1–3):251–266

    Article  CAS  PubMed  Google Scholar 

  • Drake BG, Gonzalez-Meler M, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Ann Rev Plant Physiol 48:609–639

    Article  CAS  Google Scholar 

  • Dvorak J, Luo MC, Yang ZL (1998) Genetic evidence on the origin of Triticum aestivum L. In: Damania AB, Valkoun J, Willcox G, Qualset CO (eds) The origins of agriculture and crop domestication. Proceedings of the Harlan symposium, ICARDA, Aleppo, pp 235–251

  • Ethier GJ, Livingston NJ (2004) Opinion: on the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Evans JR (2013) Improving photosynthesis. Plant Physiol 162:1780–1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60(8):2235–2248

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298

    Article  CAS  PubMed  Google Scholar 

  • Flexas JM, Ribas-Carbo A, Diaz-Espejo J, Galmés HO, Medrano L (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Diaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84

    Article  PubMed  Google Scholar 

  • Galmes J, Kapralov MV, Copolovici LO, Hermida-Carrera C, Niinemets Ü (2015) Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain. Photosynth Res 123(2):183–201

    Article  CAS  PubMed  Google Scholar 

  • Guadagnuolo R, Savova-Bianchi D, Felber F (2001) Gene flow from wheat (Triticum aestivum L.) to jointed goatgrass (Aegilops cylindrica Host.), as revealed by RAPD and microsatellite markers. Theor Appl Genet 103:1–8

    Article  CAS  Google Scholar 

  • Hanba YT, Miyazawa S-I, Terashima I (1999) The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm temperate forests. Funct Ecol 13:632–639

    Article  Google Scholar 

  • Havaux M, Strasser RS, Greppin H (1990) In vivo photoregulation of photochemical and nonphotochemical deactivation of photosystem II in intact plants. Plant Physiol Biochem 28:735–746

    CAS  Google Scholar 

  • Hoisington D, Khairallah M, Reeves T, Ribaut J-M, Skovmand B, Taba S, Warburton M (1999) Plant genetic resources: what can they contribute towards increased crop productivity? Proc Natl Acad Sci 96:5937–5943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbart S, Peng S, Horton P, Chen Y, Murchie EH (2007) Trends in leaf photosynthesis in historical rice varieties developed in the Philippines since 1966. J Exp Bot 58:3429–3438

    Article  CAS  PubMed  Google Scholar 

  • Hunt R (1978) The fitted curve in plant growth studies. In: Rose DA, Edwas DAC (eds) Math and plant physiology. Academic Press, London, pp 283–289

    Google Scholar 

  • Kalaji MH, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska AI, Cetner DM, Lukasik I, Goltsev V, Ladle JR (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ et al (2017) Frequently asked questions about in vivo chlorophyll fluorescence: the sequel. Photosynth Res 132:13–66

    Article  CAS  PubMed  Google Scholar 

  • Kaminski A, Austin RB, Ford MA, Morgan CL (1990) Flag leaf anatomy of Triticum and Aegilops species in relation to photosynthetic rate. Ann Bot 66:359–365

    Article  Google Scholar 

  • Kerber ER (1964) Wheat: reconstitution of the tetraploid component (AABB) of hexaploids. Science 143:253–255

    Article  CAS  PubMed  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hortic 19:13–14

    Google Scholar 

  • Kislev ME (1980) Triticum parvicoccum sp. nov., the oldest naked wheat. Israel J Bot 28:95–107

    Google Scholar 

  • Knight CA, Ackerly DD (2002) An ecological and evolutionary analysis of photosynthetic thermotolerance using the temperature-dependent increase in fluorescence. Oecologia 130:505–514

    Article  PubMed  Google Scholar 

  • Kreslavski VD, Lubimov VY, Shabnova NI, Balakhnina TI, Kosobryukhov AA (2009) Heat-induced impairments and recovery of photosynthetic machinery in wheat seedlings: role of light and prooxidant-antioxidant balance. Physiol Mol Biol Plant 15(2):115–122

    Article  CAS  Google Scholar 

  • Kubien DS, Sage RF (2008) The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. Plant Cell Environ 31(4):407–418

    Article  CAS  PubMed  Google Scholar 

  • Li X, Cai J, Liu F, Dai T, Cao W, Jiang D (2014) Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature. Funct Plant Biol 41:690–703

    Article  CAS  Google Scholar 

  • Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54(392):2393–2401

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330

    Article  CAS  PubMed  Google Scholar 

  • Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka Y, Nasuda S (2004) Durum wheat as a candidate for the unknown female progenitor of bread wheat: an empirical study with a highly fertile F1 hybrid with Aegilops tauschii Coss. Theor Appl Genet 109:1710–1717

    Article  PubMed  Google Scholar 

  • McFadden ES, Sears ER (1946) The origin of Triticum spelta and its free-threshing hexaploid-relatives. J Hered 37:107–116

    Article  Google Scholar 

  • Mitchell RAC, Black CR, Burkart S, Burke JI, Donnelly A, De Temmmerman L, Fangmeier A, Mulholland BJ, Theobald JC, van Oijen M (1999) Photosynthetic responses in spring wheat grown under elevated CO2 concentrations and stress conditions in the European, multiple-site experiment ‘ESPACE-wheat’. Eur J Agron 10:205–214

    Article  Google Scholar 

  • Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94:217–224

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • Neuner G, Pramsohler M (2006) Freezing and high temperature thresholds of photosystem 2 compared to ice nucleation, frost and heat damage in evergreen subalpine plants. Physiol Plant 126:196–204

    Article  CAS  Google Scholar 

  • Niinemets Ü, Diaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  CAS  PubMed  Google Scholar 

  • Olsovska K, Kovar M, Brestic M, Zivcak M, Slamka P, Shao HB (2016) Genotypically identifying wheat mesophyll conductance regulation under progressive drought stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01111

    PubMed  PubMed Central  Google Scholar 

  • Parry MAJ, Madgwick PJ, Carvalho JFC, Andralojc PJ (2007) Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. J Agr Sci 145:31–43

    Article  CAS  Google Scholar 

  • Peet MM, Kramer PJ (1980) Effects of decreasing source-sink ratio in soybeans on photosynthesis, photorespiration, transpiration and yield. Plant Cell Environ 3:201–206

    Google Scholar 

  • Pons TL, Flexas J, von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (1999) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60:2217–2234

    Article  Google Scholar 

  • Radford PJ (1967) Growth analysis formula, their uses and abuses. Crop Sci 7:171–175

    Article  Google Scholar 

  • Reynolds NP, Martin JM, Giroux MJ (2010) Increased wheat grain hardness conferred by novel puroindoline haplotypes from Aegilops tauschii. Crop Sci 50:1718–1727

    Article  CAS  Google Scholar 

  • Reynolds M, Bonnett D, Chapman SC, Furbank RT, Manès Y, Mather DE, Parry MA (2011) Raising yield potential of wheat. Overview of a consortium approach and breeding strategies. J Exp Bot 62:439–452

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Smale M, Ortiz-Monasterio I, Warburton M, Skovmand B, Reynolds M, Crossa J, Singh R, Trethowan R (2002) Dimensions of diversity in modern spring bread wheat in developing countries from 1965. Crop Sci 42:1766–1779

    Article  Google Scholar 

  • Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255

    Article  CAS  PubMed  Google Scholar 

  • Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Evans JR, Chow WS (1994) Changes in the photosynthetic properties of Australian wheat cultivars over the last century. Aust J Plant Physiol 21:169–183

    Article  CAS  Google Scholar 

  • Zhu XG, Portis AR, Long SP (2004) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165

    Article  CAS  Google Scholar 

  • Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Olsovska K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil Environ 54(4):133–139

    Article  Google Scholar 

  • Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117(1–3):529–546

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the projects VEGA-1-0923-16, VEGA-1/0831/17, APVV-15-0721, APVV SK-BG-2013-0029, and APVV SK-CN-2015-0005, and by the Grants from Russian Foundation for Basic Research (Nos: 17-04-01289; 17-54-7819), and by Molecular and Cell Biology Programs from Russian Academy of Sciences.

Author information

Author notes

  1. Marian Brestic and Marek Zivcak have contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Physiology, Slovak Agricultural University, Tr. A. Hlinku 2, 949 76, Nitra, Slovakia

    Marian Brestic & Marek Zivcak

  2. National Agricultural and Food Centre, Research Institute of Plant Production, Piešťany, Slovakia

    Pavol Hauptvogel

  3. Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. Georgi Bonchev Street, Bldg. 21, 1113, Sofia, Bulgaria

    Svetlana Misheva & Konstantina Kocheva

  4. State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China

    Xinghong Yang

  5. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China

    Xiangnan Li

  6. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, Russia, 127276

    Suleyman I. Allakhverdiev

  7. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia, 142290

    Suleyman I. Allakhverdiev

  8. Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow, Russia, 119991

    Suleyman I. Allakhverdiev

  9. Moscow Institute of Physics and Technology, Institutsky lane 9, Dolgoprudny, Moscow Region, Russia, 141700

    Suleyman I. Allakhverdiev

  10. Institute of Molecular Biology and Biotechnology, Azerbaijan National Academy of Sciences, Matbuat Avenue 2a, 1073, Baku, Azerbaijan

    Suleyman I. Allakhverdiev

Authors
  1. Marian Brestic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marek Zivcak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pavol Hauptvogel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Svetlana Misheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Konstantina Kocheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xinghong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiangnan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Suleyman I. Allakhverdiev
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MZ, MB, and SIA wrote the paper. MZ conducted the statistical analyses and analyses of photosynthetic parameters. PH provided unique biological material and led the field experiments. SM, KK, XY, and XL contributed to experimental design and interpretation of results, and helped to draft the manuscript. Neither the manuscript nor any part of its content has been published or submitted for publication elsewhere. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Marian Brestic or Suleyman I. Allakhverdiev.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brestic, M., Zivcak, M., Hauptvogel, P. et al. Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynth Res 136, 245–255 (2018). https://doi.org/10.1007/s11120-018-0486-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-018-0486-z

Keywords

Search

Navigation