Skip to main content
SpringerLink
Log in

Cold Tolerance of the Photosynthetic Apparatus: Pleiotropic Relationship between Photosynthetic Performance and Specific Leaf Area of Maize Seedlings

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

The objective of this study was to elucidate the genetic relationship between the specific leaf area (SLA) and the photosynthetic performance of maize (Zea mays L.) as dependent on growth temperature. Three sets of genotypes: (i) 19 S5 inbred lines, divergently selected for high or low operating efficiency of photosystem II (ΦPSII) at low temperature, (ii) a population of 226 F 2:3 families from the cross of ETH-DL3 × ETH-DH7, and (iii) a population of 168 F 2:4 families from the cross of Lo964 × Lo1016 were tested at low (15/13 °C day/night) or at optimal (25/22 °C day/night) temperature. The latter cross was originally developed to study QTLs for root traits. At 15/13 °C the groups of S5 inbred lines selected for high or low ΦPSII differed significantly for all the measured traits, while at optimal temperature the groups differed only with regard to leaf greenness (SPAD). At low temperature, the SLA of these inbred lines was negatively correlated with ΦPSII (r = − 0.56, p < 0.05) and SPAD (r = − 0.80, p < 0.001). This negative relationship was confirmed by mapping quantitative trait loci (QTL) in the two mapping populations. A co-location of three QTLs for SLA with QTLs for photosynthesis-related traits was detected in both populations at 15/13 °C, while co-location was not detected at 25/22 °C. The co-selection of SLA and ΦPSII in the inbred lines and the co-location of QTL for SLA, SPAD, and ΦPSII at 15/13 °C in the QTL populations strongly supports pleiotropy. There was no evidence that selecting for high ΦPSII at low temperature leads to a constitutively altered SLA.

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

Similar content being viewed by others

Abbreviations

CER:

carbon exchange rate

ΦPSII :

operating efficiency of photosystem II

PPFD:

photosynthetic photon flux density

QTL:

quantitative trait locus

SLA:

specific leaf area

SPAD:

soil plant analysis development, leaf greenness

References

  1. O.K. Atkin H. Lambers (1998) Slow-growing alpine and fast-growing lowland species: a case study of factors associated with variation in growth rate among herbaceous higher plants under natural and controlled conditions H. Lambers H. Poorter M.M.I. Van Vuuren (Eds) Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences Backhuys Publishers Leiden

    Google Scholar 

  2. J.R. Evans (1998) Photosynthetic characteristics of fast- and slow-growing species H. Lambers H. Poorter M.M.I. Van Vuuren (Eds) Inherent Variation in Plant Growth Physiological Mechanisms and Ecological Consequences Backhuys Publishers Leiden 101–119

    Google Scholar 

  3. J.R. Evans H. Poorter (2001) ArticleTitlePhotosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain Plant Cell Environ. 24 755–767 Occurrence Handle1:CAS:528:DC%2BD3MXmsFCmurk%3D

    CAS  Google Scholar 

  4. K. Fichtner W.P. Quick E.-D. Schulze H.A. Mooney S.R. Rodermel L. Bogorad M. Stitt (1993) ArticleTitleDecreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ȁ8antisenseȁ9 rbcS. V. Relationship between photosynthetic ratestorage strategy, biomass allocation and vegetative plant growth at three different nitrogen supplies Planta 190 1–9 Occurrence Handle1:CAS:528:DyaK3sXktVCqu7k%3D

    CAS  Google Scholar 

  5. Y. Fracheboud (1999) Cold adaptation of the photosynthetic apparatus of maize by growth at suboptimal temperature M. Sanches-Diaz J.J. Irigoyen J. Aguirreola K. Pithan (Eds) Crop Developement for the Cool and Wet Climate of Europe Office for the Official Publications of the European Communities Brussels 88–89

    Google Scholar 

  6. Y. Fracheboud P. Haldimann J. Leipner P. Stamp (1999) ArticleTitleChlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.) J. Exp. Bot. 50 1533–1540 Occurrence Handle1:CAS:528:DyaK1MXmtlamtLY%3D

    CAS  Google Scholar 

  7. Y. Fracheboud C. Jompuk J.-M. Ribaut P. Stamp J. Leipner (2004) ArticleTitleGenetic analysis of cold-tolerance of the photosynthesis in maize Plant Mol. Biol. 56 241–253 Occurrence Handle15604741 Occurrence Handle1:CAS:528:DC%2BD2MXhtVektg%3D%3D

    PubMed  CAS  Google Scholar 

  8. B. Genty J.-M. Briantais N.R. Baker (1989) ArticleTitleThe relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence Biochim. Biophys. Acta 990 87–92 Occurrence Handle1:CAS:528:DyaL1MXhsFWntL4%3D

    CAS  Google Scholar 

  9. A. Hund Y. Frachboud A. Soldati E. Frascaroli S. Salvi P. Stamp (2004) ArticleTitleQTL controlling root and shoot traits of maize seedlings under cold stress Theor. Appl. Genet. 109 618–629 Occurrence Handle15179549 Occurrence Handle1:CAS:528:DC%2BD2cXmt1Krs7w%3D

    PubMed  CAS  Google Scholar 

  10. R. Ihaka R. Gentleman (1996) ArticleTitleR: a language for data analysis and graphics J. Comput. Graph. Stat. 5 299–314

    Google Scholar 

  11. R.C. Jansen P. Stam (1994) ArticleTitleHigh resolution of quantitative traits into multiple loci via interval mapping Genetics 136 1447–1455 Occurrence Handle8013917 Occurrence Handle1:STN:280:DyaK2c3otl2jug%3D%3D

    PubMed  CAS  Google Scholar 

  12. C. Jiang Z.B. Zeng (1995) ArticleTitleMultiple trait analysis of genetic mapping for quantitative trait loci Genetics 140 111–127

    Google Scholar 

  13. E.A. Lee M.A. Staebler M. Tollenaar (2002) ArticleTitleGenetic variation and physiological discrimination for cold tolerance in maize (Zea Mays L.) during an early autotrophic phase of development Crop Sci. 42 1919–1929

    Google Scholar 

  14. J. Leipner A. Stehli A. Soldati (1999) ArticleTitlePhotosynthetic performance of exotic maize (Zea mays L.) germplasm from tropical highlands at low and high temperature J. Appl. Bot. 73 20–24 Occurrence Handle1:CAS:528:DyaK1MXjvFahsrc%3D

    CAS  Google Scholar 

  15. C. Lopez-Castaneda R.A. Richards G.D. Farquhar (1995) ArticleTitleVariation in early vigour between wheat and barley Crop Sci. 35 472–479 Occurrence Handle10.2135/cropsci1995.0011183X003500020032x

    Article  Google Scholar 

  16. H. Poorter A. Van der Werf (1998) Is inherent variation in RGR deTermined by LAR at low irradiance and by NAR at high irradiance* A review of herbaceous species H. Lambers H. Poorter M.M.I. Van Vuuren (Eds) Inherent Variation in Plant Growth Physiological Mechanisms and Ecological Consequences Backhuys Publishers Leiden 309–332

    Google Scholar 

  17. T.K. Prasad (1997) ArticleTitleRole of catalase in lnducing chilling tolerance in pre-emergent maize seedlings Plant Physiol. 114 1369–1376 Occurrence Handle12223775 Occurrence Handle1:CAS:528:DyaK2sXlsleisbk%3D

    PubMed  CAS  Google Scholar 

  18. W.P. Quick (1998) Transgenic plants as a tool to analyse the mechanistic basis for variation in plant growth H. Lambers H. Poorter M.M.I. Van Vuuren (Eds) Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences Backhuys Publishers Leiden 199–219

    Google Scholar 

  19. R.A. Richards (2000) ArticleTitleSelectable traits to increase crop photosynthesis and yield of grain crops J. Exp. Bot. 51 447–458 Occurrence Handle10938853 Occurrence Handle1:CAS:528:DC%2BD3cXhsVOjsrw%3D

    PubMed  CAS  Google Scholar 

  20. Ritchie S.W. and Hanway J.J. 1984. How a corn plant develops. Special Report No. 48. Cooperative Extension ServiceAmes. http://maize.agron.iastate.edu/corngrows.html.

  21. L. Rizhsky E. Hallak-Herr F. Van Breusegem S. Rachmilevitch J.E. Barr S. Rodermel D. Inzé R. Mittler (2002) ArticleTitleDouble antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase Plant J. 32 329–342 Occurrence Handle12410811 Occurrence Handle1:CAS:528:DC%2BD38Xpt12msrY%3D

    PubMed  CAS  Google Scholar 

  22. M.C. Sanguineti M.M. Giuliani G. Govi R. Tuberosa P. Landi (1998) ArticleTitleRoot and shoot traits of maize inbred lines grown in the field and in hydroponic culture and their relationship with root lodging Maydica 43 211–216

    Google Scholar 

  23. J.G. Scandalios A.S. Tsaftaris J.M. Chandlee R.W. Skadsen (1984) ArticleTitleExpression of the developmentally regulated catalase (cat) genes in maize Dev. Genet. 4 281–293 Occurrence Handle1:CAS:528:DyaL2cXls1Clt7w%3D

    CAS  Google Scholar 

  24. A. Soldati A. Stehli P. Stamp (1999) ArticleTitleTemperature adaptation of tropical highland maize (Zea mays L.) during early growth and in controlled conditions Europ. J. Agron. 10 111–117

    Google Scholar 

  25. A. Stehli A. Soldati P. Stamp (1999) ArticleTitleVegetative performance of tropical highland maize (Zea mays L.) in the field J. Agron. Crop Sci. 183 193–198

    Google Scholar 

  26. C.M. Stirling G.Y. Nie C. Aguilera A. Nugawela S.P. Long N.R. Baker (1991) ArticleTitlePhotosynthetic productivity of an immature maize crop: changes in quantum yield of CO2 assimilation, conversion efficiency and thylakoid proteins Plant Cell Environ. 14 3905–3914

    Google Scholar 

  27. M. Stitt D. Schulze (1994) ArticleTitleDoes Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology Plant Cell Environ. 17 465–487 Occurrence Handle1:CAS:528:DyaK2cXlt12rsbw%3D

    CAS  Google Scholar 

  28. T. Terauchi M. Matsuoka (2000) ArticleTitleIdeal characteristics for the early growth of sugarcane Jpn. J. Crop. Sci. 69 286–292

    Google Scholar 

  29. R. Tuberosa M.C. Sanguineti P. Landi M.M. Giuliani S. Salvi S. Conti (2002) ArticleTitleIdentification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes Plant Mol. Biol. 48 697–712 Occurrence Handle11999844 Occurrence Handle1:CAS:528:DC%2BD38XjsFWrt70%3D

    PubMed  CAS  Google Scholar 

  30. M.J. Verheul C. Picatto P. Stamp (1996) ArticleTitleGrowth and development of maize seedlings under chilling conditions in the field Europ. J. Agron. 5 31–43 Occurrence Handle10.1016/S1161-0301(96)02007-2

    Article  Google Scholar 

  31. Z.B. Zeng (1994) ArticleTitlePrecision mapping of quantitative trait loci Genetics 136 1457–1468 Occurrence Handle8013918 Occurrence Handle1:CAS:528:DyaK2MXhtFantw%3D%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Plant Sciences, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, 8092, Zurich, Switzerland

    Andreas Hund, Jörg Leipner, Peter Stamp & Yvan Fracheboud

  2. Dip. Scienze e Tecnologie Agroambientali (DiSTA), Università di Bologna, Bologna, Italy

    Elisabetta Frascaroli

  3. Department of Agronomy, Kasetsart University, Phaholyothin Road, 10903, Bangkok, Thailand

    Choosak Jompuk

Authors
  1. Andreas Hund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabetta Frascaroli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jörg Leipner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Choosak Jompuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Stamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yvan Fracheboud
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Hund.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hund, A., Frascaroli, E., Leipner, J. et al. Cold Tolerance of the Photosynthetic Apparatus: Pleiotropic Relationship between Photosynthetic Performance and Specific Leaf Area of Maize Seedlings. Mol Breeding 16, 321–331 (2005). https://doi.org/10.1007/s11032-005-1642-7

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-005-1642-7

Keywords

Search

Navigation