Abstract
The genetic basis of cold-tolerance was investigated by analyzing the quantitative trait loci (QTL) of an F2:3 population derived from a cross between two lines bred for contrasting cold-tolerance using chlorophyll fluorescence as a selection tool. Chlorophyll fluorescence parameters, CO2 exchange rate, leaf greenness, shoot dry matter and shoot nitrogen content were determined in plants grown under controlled conditions at 25/22 °C or 15/13 °C (day/night). The analysis revealed the presence of 18 and 19 QTLs (LOD > 3.5) significantly involved in the variation of nine target traits in plants grown at 25/22 °C and 15/13 °C, respectively. Only four QTLs were clearly identified in both temperatures regimes for the same traits, demonstrating that the genetic control of the performance of the photosynthetic apparatus differed, depending on the temperature regime. A major QTL for the cold-tolerance of photosynthesis was identified on chromosome 6. This QTL alone explained 37.4 of the phenotypic variance in the chronic photoinhibition at low temperature and was significantly involved in the expression of six other traits, including the rate of carbon fixation and shoot dry matter accumulation, indicating that the tolerance to photoinhibition is a key factor in the tolerance of maize to low growth temperature. An additional QTL on chromosomes 2 corresponded to a QTL identified previously in another population, suggesting some common genetic basis of the cold-tolerance of photosynthesis in different maize germplasms.
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Agrama, H. A. S., Zakaria, A. G., Said, F. B. and Tuinstra, M. 1999. Identification of quantitative trait loci for nitrogen use efficiency in maize. Mol. Breeding 5: 187-195.
Andaya, V. C. and Mackill, D. J. 2003. Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J. Exp. Bot. 54: 2579-2585.
Andrews, J. R., Fryer, M. J. and Baker, N. R. 1995. Characterisation of chilling effects on photosynthetic performance of maize crops during early season growth using chlorophyll fluorescence. J. Exp. Bot. 46: 1195-1203.
Baroja-Fernandez, E., Munoz, F. J., Akazawa, T. and PozuetaRomero, J. 2001. Reappraisal of the currently prevailing model of starch biosynthesis in photosynthetic tissues: a proposal involving the cytosolic production of ADP-glucose by sucrose synthase and occurrence of cyclic turnover of starch in the chloroplast. Plant Cell Physiol. 42: 1311-1320.
Basten, C. J., Weir, B. S. and Zeng, Z. B. 1994. Zmap-a QTL Cartographer. In: C. Smith, J. S. Gavora, B. Benkel, J. Chesnais, W. Fairfull, J. P. Gibson, B. W. Kennedy and E. B. Burnside (Eds.), Proceedings of the 5th World Congress on Genetics Applied to Livestock Production: Computing Strategies and Software. Organizing Committee, 5th World Congress on Genetics Applied to Livestock Production, Guelph, pp. 65-66.
Basten, C. J., Weir, B. S. and Zeng, Z. B. 2002. QTL Cartographer, A Reference Manual and Tutorial for QTL Mapping. Department of Statistics, North Carolina State University, Raleigh.
Brutnell, T. P., Sawers, R. J. H., Mant, A. and Langdale, J. A. 1999. BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11: 849-864.
Fracheboud, Y., Haldimann, P., Leipner, J. and Stamp, P. 1999. Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). J. Exp. Bot. 50: 1533-1540.
Fracheboud, Y., Ribaut, J.-M., Vargas, M., Messmer, R. and Stamp, P. 2002. Identification of quantitative trait loci for cold-tolerance of photosynthesis in maize (Zea mays L.). J. Exp. Bot. 53: 1967-1977.
Genty, B., Briantais, J.-M. and Baker, N. R. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta. 990: 87-92.
Haldimann, P. 1998. Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity. Plant Cell Environ. 21: 200-208.
Haldimann, P., Fracheboud, Y. and Stamp, P. 1995. Carotenoid composition in Zea mays developed at sub-optimal temperature and different light intensities. Physiol. Plant. 95: 409-414.
Hattenbach, A., Mu ¨ller-Ro ¨ber, B., Nast, G. and Heineke, D. 1997. Antisense repression of both ADP-glucose pyrophosphorylase and triose phosphate translocator modifies carbohydrate partitioning in potato leaves. Plant Physiol. 115: 471-475.
Hirel, B., Bertin, P., Quillere, I., Bourdoncle, W., Attagnant, C., Dellay, C., Gouy, A., Cadiou, S., Retailliau, C., Falque, M. and Gallais, A. 2001. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol. 125: 1258-1270.
Hoisington, D., Khairallah, M. and Gonza ´lez-de-Leo ´n, D. 1994. Laboratory Protocols: CIMMYT Applied Molecular Genetics Laboratory. CIMMYT, Mexico, D. F.
Joliot, P. and Joliot, A. 1964. Etudes cine ´tiques de la re ´action photochimique libe ´rant l 'oxyge`ne au cours de la photosynthe`se. Compte rendu Acade ´mie Sciences Paris 258: 4622-4625.
Kingston-Smith, A. H., Harbinson, J., Williams, J. and Foyer, C. H. 1997. Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photo-inhibition in maize leaves. Plant Physiol. 114: 1039-1046.
Kraja, A. T. and Dudley, J. W. 2000. QTL analysis of two maize inbred line crosses. Maydica 45: 1-12.
Krause, G. H. 1988. Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74: 566-574.
Kubien, D. S., von Cammerer, S., Furbank, R. T. and Sage, R. F. 2003. C-4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol. 132: 1577-1585.
Lander, E. S., Green, P., Abrahamson, J., Barlow, A., Daly, M. J., Lincoln, S. E. and Newburg, L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174-181.
Lee, E. A., Staebler, M. A. and Tollenaar, M. 2002. Genetic variation in physiological discriminators for cold tolerance-early autotrophic phase of maize development. Crop Sci. 42: 1919-1929.
Leipner, J., Fracheboud, Y. and Stamp, P. 1999. Effect of growing season on the photosynthetic apparatus and leaf antioxidative defences in two maize genotypes of different chilling tolerance. Environ. Exp. Bot. 42: 129-139.
Miedema, P. 1982. The effects of low temperature on Zea mays. Adv. Agron. 35: 93-128.
Moon, H. G., Brewbaker, J. L. and Lu, X. W. 1999. Major QTLs for disease resistance and other traits identified in recombinant inbred lines from tropical maize hybrids. Maydica 44: 301-311.
Nie, G. Y. and Baker, N. R. 1991. Modifications to thylakoid composition during. development of maize leaves at low growth temperatures. Plant Physiol. 95: 184-191.
Ortiz-Lopez, A., Nie, G. Y., Ort, D. and Baker, N. R. 1990. The involvement of the photoinhibition of photosystem II and impaired membrane-energizationinthe reduced quantumyield of carbon assimilation in chilled maize. Planta 181: 78-84.
Purcell, L. C., Ashley, D. A. and Boerma, H. R. 1987. Effects of chilling on photosynthetic capacity, and leaf carbohydrate and nitrogen status of soybean. Crop Sci. 27: 90-95.
Ribaut, J.-M., Baenziger, M., Setter, T., Edmeades, G. and Hoisington, D. 2004. Genetic dissection of drought tolerance in maize: a case study. In: H. Nguyen and A. Blum (Eds.), Physiology and Biotechnology Integration for Plant Breeding. Marcel Dekker, Inc., New York, 571-609.
Robertson, E. J., Baker, N. R. and Leech, R. M. 1993. Chloroplast thylakoid protein changes induced by low growth temperature in maize revealed by immunocytology. Plant Cell Environ. 16: 809-818.
Rosenqvist, E. and van Kooten, O. 2003. Chlorophyll fluorescence: a general description and nomenclature. In: J. R. DeEll, and P. M. A. Toivonen, (Eds.), Practical Applications of Chlorophyll Fluorescence in Plant Biology. Kluwer Academic Publishers, Dordrecht, pp. 31-77.
Stirling, C. M., Nie, G. Y., Aguilera, C., Nugawela, A., Long, S. P. and Baker, N. R. 1991. Photosynthetic productivity of an immature maize crop-changes in quantum yield of CO2 assimilation, conversion efficiency and thylakoid proteins. Plant Cell Environ. 14: 947-954.
Sun, J. D., Okita, T. W. and Edwards, G. E. 1999. Modification of carbon partitioning, photosynthetic capacity, and O2 sensitivity in arabidopsis plants with low ADP-glucose pyrophosphorylase activity. Plant Physiol. 119: 267-276.
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Fracheboud, Y., Jompuk, C., Ribaut, J.M. et al. Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Mol Biol 56, 241–253 (2004). https://doi.org/10.1007/s11103-004-3353-6
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DOI: https://doi.org/10.1007/s11103-004-3353-6