Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
REVIEW

Chilling tolerance in maize: agronomic and physiological approaches

Muhammad Farooq A E , Tariq Aziz A , Abdul Wahid B , Dong-Jin Lee C and Kadambot H. M. Siddique D

A Department of Agronomy, University of Agriculture, Faisalabad-38040, Pakistan.

B Department of Botany, University of Agriculture, Faisalabad-38040, Pakistan.

C Department of Crop Science and Biotechnology, Dankook University, Chungnam-330-714, Korea.

D Institute of Agriculture, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, WA 6009, Australia.

E Corresponding author. Email: farooqcp@gmail.com

Crop and Pasture Science 60(6) 501-516 https://doi.org/10.1071/CP08427
Submitted: 2 December 2008  Accepted: 16 March 2009   Published: 12 June 2009

Abstract

Maize is a C4 plant species with higher temperature optima than C3 plant species. Growth and productivity of maize are severely constrained by chilling stress. Here, we review the effects of chilling stress on growth, phenology, water and nutrient relations, anatomy, and photosynthesis in maize. Several management strategies to cope with chilling stress are also proposed. In maize, chilling stress is known to reduce leaf size, stem extension and root proliferation, disturb plant water relations, and impede nutrient uptake. Chilling stress in maize is a complex phenomenon with physiological and biochemical responses at both cellular and whole-organ level. CO2 assimilation by leaves is reduced mainly due to membrane damage, photoinhibition, and disturbed activity of various enzymes. Enhanced metabolite flux through the photorespiratory pathway increases the oxidative load on tissues as both processes generate reactive oxygen species (ROS). Injury caused by ROS to macromolecules under chilling stress is one of the major deterrents to growth. Low-molecular-weight osmolytes, including glycinebetaine, proline, and organic acids, are crucial in sustaining cellular function under chilling stress. Plant growth substances such as salicylic acid, gibberellic acid, and abscisic acid modulate the response of maize to chilling stress. Polyamines and several enzymes act as antioxidants and reduce the adverse effects of chilling stress. Chilling tolerance in maize can be managed through the development and selection of chilling-tolerant genotypes by breeding and genomic approaches. Agronomic approaches such as exogenous application of growth hormones and osmoprotectants to seeds or plants, and early vigour, can also aid in chilling tolerance.

Additional keywords: chilling response, stomatal oscillation, osmoprotectants, hormones, stress proteins, chilling management, CO2.


References


Aguilera C, Stirling CM, Long SP (1999) Genotypic variation within Zea mays L. for susceptibility to and rate of recovery from chill-induced photoinhibition of photosynthesis. Plant Physiology 106, 429–436.
CrossRef | CAS | open url image1

Ahmad I, Hellebust JA (1988) The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiology 88, 348–354.
CrossRef | CAS | PubMed | open url image1

Alberda T (1969) The effect of low temperature on dry matter reduction, chlorophyll concentration and photosynthesis of maize plants of different ages. Acta Botantica Nederlandica 18, 39–49.
CAS |
open url image1

Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm climate plants. Trends in Plant Science 6, 36–42.
CrossRef | CAS | PubMed | open url image1

Anderson MD, Prasad TK, Martin BA, Steward CR (1994) Differential gene expression in chilling-acclimated maize seedlings and evidence for the involvement of abscisic acid in chilling tolerance. Plant Physiology 105, 331–339.
CAS | PubMed |
open url image1

Anon. (2009) Vegetable Program Glossary. Available at: www.usask.ca/agriculture/plantsci/vegetable/definition.htm (accessed 5 Feb. 2009)

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
CrossRef | CAS | PubMed | open url image1

Arakawa T, Timasheff SN (1983) Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Archives of Biochemistry and Biophysics 224, 169–177.
CrossRef | CAS | PubMed | open url image1

Aroca R, Vernieri P, Irigoyen JJ, Sancher-Diaz M, Tognoni F, Pardossi A (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Science 165, 671–679.
CrossRef | CAS | open url image1

Ashraf M, Foolad MR (2007) Roles of glycinebetaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206–216.
CrossRef | CAS | open url image1

Baker NR (1996) Photoinhibition of photosynthesis. In ‘Light as an energy source and information carrier in plant physiology’. (Eds RC Jennings, G Zucchelli, F Ghetti, G Colombetti) pp. 89–97. (Plenum Press: New York)

Baker NR, Bradbury M, Farage PK, Ireland CR, Long SP (1989) Measurements of quantum yield of carbon assimilation and chlorophyll fluorescence for assessment of photosynthetic performance of crop plants in the field. Philosophical Transactions of the Royal Society 323, 295–308.
CrossRef | CAS | open url image1

Baker NR, East TM, Long SP (1983) Chilling damage to photosynthesis in young Zea mays. 2. Photochemical function of thylakoids in vivo. Journal of Experimental Botany 34, 189–197.
CrossRef | CAS | open url image1

Baker NR , Nie GY (1994) Chilling sensitive of photosynthesis in maize. In ‘Biotechnology in agriculture and forestry, Vol. 9’. (Ed. YPS Bajaj) pp. 465–481. (Springer-Verlag: Berlin)

Barlow PW, Adam JS (1989) Anatomical disturbances in primary roots of Zea mays following periods of cool temperature. Environmental and Experimental Botany 29, 323–336.
CrossRef | open url image1

Barloy J (1983) Phase germination, levee implantation. In ‘Physiology of maize’. (Ed. A Gallais) (INRA: Pau, France)

Basra AS, Bedi S, Malik CP (1988) Pre-sowing hydration of maize seeds for stimulation of low-temperature germination and its effects on phospholipid changes in the embryos. Current Science 57, 1340–1342. open url image1

Basra SMA, Farooq M, Wahid A, Khan MB (2006) Rice seed invigoration by hormonal and vitamin priming. Seed Science and Technology 34, 775–780. open url image1

Bateman JB, Evans GF, Brown PR, Gabriel C, Grant EH (1992) Dielectric properties of the system bovine albumin urea betaine in aqueous solution. Physics in Medicine and Biology 37, 175–182.
CrossRef | CAS | PubMed | open url image1

Ben-Haj-Salah H, Tardieu F (1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length. Plant Physiology 109, 861–870.
CAS | PubMed |
open url image1

Benjamin LR (1990) Variation in time of seedling emergence within populations. Advances in Agronomy 44, 1–25.
CrossRef | open url image1

Blacklow WM (1972) Influence of temperature on germination and elongation of the radicle and shoot of corn (Zea mays L.). Crop Science 12, 647–650. open url image1

Blum A (1988) ‘Plant breeding for stress environments.’ (CRC Press Inc.: Boca Raton, FL)

Bohnert HJ, Jensen RG (1996) Metabolic engineering for increased salt tolerance the next step. Australian Journal of Plant Physiology 23, 661–666. open url image1

Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187, 348–358.
CrossRef | CAS | open url image1

Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Science 140, 103–125.
CrossRef | CAS | open url image1

Bowen G (1991) Soil temperature, root growth, and plant function. In ‘Plant roots the hidden half’.’ (Ed. Y Waisel) (Marcel Dekker, Inc.: New York)

Bravo-F P, Uribe EG (1981) Temperature dependence of the concentration kinetics of absorption of phosphate and potassium in corn roots. Plant Physiology 67, 815–819.
CrossRef | CAS | PubMed | open url image1

Bret-Harte MS, Silk WK (1994) Fluxes and deposition rates of solutes in growing roots of Zea mays L. Journal of Experimental Botany 45, 1733–1742.
CAS |
open url image1

Bristow KL (1988) The role of mulch and its architecture in modifying soil temperature. Australian Journal of Soil Research 26, 269–280.
CrossRef | open url image1

Brugière N, Dubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, Hirel B (1999) Glutamine synthetase in the phloem plays a major role in controlling proline production. The Plant Cell 11, 1995–2011.
CrossRef | PubMed |
open url image1

Cao DD, Hu J, Gao CH, Guan YJ, Zhang S, Xiao JF (2008) Chilling tolerance of maize (Zea mays L.) can be improved by seed soaking in putrescine. Seed Science and Technology 36, 191–197. open url image1

Carey RW, Berry JA (1978) Effects of low temperature on respiration and uptake of rubidium ions by excised barley and corn roots. Plant Physiology 61, 858–860.
CrossRef | CAS | PubMed | open url image1

Chu TM, Jusaitis M, Aspinall D, Paleg LG (1978) Accumulation of free proline at low temperatures. Physiologia Plantarum 43, 254–260.
CrossRef | CAS | open url image1

Clarkson DT , Earnshaw MJ , White PJ , Cooper HD (1988) Temperature dependent factors influencing nutrient uptake: an analysis of responses at different levels of organization. In ‘Plants and temperature’. (Eds SP Long, FI Woodward). Symposium of the Society of Experimental Biologists 42, 281–309.

Coughlan SJ, Heber U (1982) The role of glycinebetaine in the protection of spinach thylakoids against freezing stress. Planta 156, 62–69.
CrossRef | CAS | open url image1

Cutforth HW, Shaykewich CF, Cho CM (1986) Effect of soil water and temperature on corn (Zea mays L.) root growth during emergence. Canadian Journal of Soil Science 66, 51–58. open url image1

Daie J, Campbell WF, Seeley SS (1981) Temperature-stress-induced production of abscisic acid and dihydrophaseic acid in warm- and cool-season crops. Journal of the American Society for Horticultural Science 106, 11–13.
CAS |
open url image1

de Juan Javier P, Jose IJ, Manuel S-D (1997) Chilling of drought-hardened and non-hardened plants of different chilling-sensitive maize lines. Changes in water relations and ABA contents. Plant Science 122, 71–79.
CrossRef | CAS | open url image1

Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. The Plant Journal 4, 215–223.
CrossRef | CAS | open url image1

Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiology 114, 1031–1037.
CAS | PubMed |
open url image1

Dubey RS (1999) Protein synthesis by plants under stressful conditions. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakli) pp. 365–397. (Marcel Dekker, Inc.: New York)

Duncan WG, Hesketh JD (1968) Net photosynthesis rates, relative leaf growth rates, and leaf numbers of 22 races of maize grown at eight temperatures. Crop Science 8, 670–674. open url image1

Dwivedi SL, Crouch JH, Mackill DJ, Xu Y, Blair MW, Ragot M, Upadhyaya HD, Ortiz R (2007) The molecularization of public sector crop breeding: progress, problems, and prospects. Advances in Agronomy 95, 163–318.
CrossRef | CAS | open url image1

Enns LC, McCully ME, Canny MJ (2006) Branch roots of young maize seedlings, their production, growth, and phloem supply from the primary root. Functional Plant Biology 33, 391–399.
CrossRef | open url image1

Evert RF, Russin WA, Bosabalidis AM (1996) Anatomical and ultrastructural changes associated with sink-tosource transition in developing maize leaves. International Journal of Plant Sciences 157, 247–261.
CrossRef | open url image1

FAOSTAT (2007) FAOSTAT. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor (accessed 23 Oct. 2008).

Farage PK , Long SP (1987) Damage to maize photosynthesis in the field during periods when chilling is combined with high photon fluxes. In ‘Progress in photosynthesis research, Vol. 4’. (Ed. J Biggins) pp. 139–142. (Martinus Nijhoff: Dordrecht, The Netherlands)

Farooq M, Aziz T, Basra SMA, Cheema MA, Rehman H (2008c) Chilling tolerance in hybrid maize induced by seed priming with salicylic acid. Journal of Agronomy and Crop Science 194, 161–168.
CrossRef | CAS | open url image1

Farooq M, Aziz T, Basra SMA, Wahid A, Khaliq A, Cheema MA (2008d) Exploring the role of calcium to improve chilling tolerance in hybrid maze. Journal of Agronomy and Crop Science 194, 350–359.
CrossRef | open url image1

Farooq M, Aziz T, Cheema ZA, Khaliq A, Hussain M (2008e) Activation of antioxidant system by KCl treatments improves the chilling tolerance in hybrid maize. Journal of Agronomy and Crop Science 194, 438–448. open url image1

Farooq M, Aziz T, Hussain M, Rehman H, Jabran K, Khan MB (2008b) Glycinebetaine improves chilling tolerance in hybrid maize. Journal of Agronomy and Crop Science 194, 152–160.
CrossRef | CAS | open url image1

Farooq M, Basra SMA, Hafeez K (2006c) Seed invigoration by osmohardening in fine and coarse rice. Seed Science and Technology 34, 181–187. open url image1

Farooq M, Basra SMA, Khalid M, Tabassum R, Mehmood T (2006d) Nutrient homeostasis, reserves metabolism and seedling vigor as affected by seed priming in coarse rice. Canadian Journal of Botany 84, 1196–1202.
CrossRef | CAS | open url image1

Farooq M, Basra SMA, Rehman H, Saleem BA (2008a) Seed priming enhances the performance of late sown wheat (Triticum aestivum L.) by improving the chilling tolerance. Journal of Agronomy and Crop Science 194, 55–60.
CrossRef | open url image1

Farooq M, Basra SMA, Tabassum R, Afzal I (2006a) Enhancing the performance of direct seeded fine rice by seed priming. Plant Production Science 9, 446–456.
CrossRef | open url image1

Farooq M, Basra SMA, Wahid A (2006b) Priming of field-sown rice seed enhances germination, seedling establishment, allometry and yield. Plant Growth Regulation 49, 285–294.
CrossRef | CAS | open url image1

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29, 185–212.
CrossRef | open url image1

Fennell A, Markhart AH (1998) Rapid acclimation of root hydraulic conductivity to low temperature. Journal of Experimental Botany 49, 879–884.
CrossRef | CAS | open url image1

Follman H (2000) Light–dark thioredoxin-mediated metabolic redox control in plant cell. In ‘The redox state and circadian rhythms’. (Ed. TD Vanden) pp. 59–85. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Fortin MC, Pierce FJ (1991) Timing and nature of much retardation of corn vegetative development. Agronomy Journal 83, 258–263. open url image1

Foyer CH, Fletcher JM (2001) Plant antioxidants colour me healthy. Biologis 48, 115–120.
CAS |
open url image1

Foyer CH, Vanacker H, Gomez LD, Harbinson J (2002) Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures. Plant Physiology and Biochemistry [review] 40, 659–668.
CrossRef | CAS | open url image1

Fracheboud Y , Haldimann P (1994) Photosynthetic traits of maize during early development in the field. In ‘Crop adaptation to cool climates’. (Eds K Dorffling, B Brettschneider, H Tantau, K Pithan) pp. 467–474. (ECSP-EEC-EAEC: Brussels)

Fracheboud Y, Haldimann P, Leipner J, Stamp P (1999) Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany 50, 1533–1540.
CrossRef | CAS | open url image1

Fracheboud Y, Jompuk C, Ribaut J-M, Stamp P, Leipner J (2004) Genetic analysis of cold tolerance of photosynthesis in maize. Plant Molecular Biology 56, 241–253.
CrossRef | CAS | PubMed | open url image1

Fracheboud Y, Ribaut J-M, Vargas M, Messmer R, Stamp P (2002) Identification of quantitative trait loci for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany 53, 1967–1977.
CrossRef | CAS | PubMed | open url image1

Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
CrossRef | CAS | PubMed | open url image1

Fryer MJ, Oxborough K, Martin B, Ort DR, Baker NR (1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Physiology 108, 761–767.
CAS | PubMed |
open url image1

Gamalei YV, van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194, 443–453.
CrossRef | CAS | open url image1

Giauffret C, Bonhomme R, Derieux M (1995) Genotypic differences for temperature response of leaf appearance rate and leaf elongation rate in field-grown maize. Agronomie 15, 123–137.
CrossRef | open url image1

Glass ADM (1983) Regulation of ion transport. Annual Review of Plant Physiology 34, 311–326.
CrossRef | CAS | open url image1

Greaves JA (1996) Improving suboptimal temperature tolerance in maize-the search for variation. Journal of Experimental Botany 47, 307–323.
CrossRef | CAS | open url image1

Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34, 35–45.
CrossRef | CAS | PubMed | open url image1

Guan L, Scandalios JG (1995) Developmentally related responses of maize catalase genes to salicylic acid. Proceedings of the National Academy of Sciences of the United States of America 92, 5930–5934.
CrossRef | CAS | PubMed | open url image1

Haldimann P (1997) Chilling-induced changes to carotenoid composition, photosynthesis. II. Photochemistry in two maize genotypes differing in tolerance to low temperature. Journal of Plant Physiology 151, 610–619.
CAS |
open url image1

Haldimann P (1998) Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays L. genotypes differing in chilling sensitivity. Plant, Cell & Environment 21, 200–208.
CrossRef | CAS | open url image1

Haldimann P (1999) how do changes in temperature during growth affect leaf pigment composition and photosynthesis in Zea mays genotypes differing in sensitivity to low temperature. Journal of Experimental Botany 50, 543–550.
CrossRef | CAS | open url image1

He YL, Liu YL, Cao WX, Huai MF, Xu BG, Huang BR (2005) Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass. Crop Science 45, 988–995.
CrossRef | CAS | open url image1

Hetherington SE, Öquist G (1988) Monitoring chilling injury: a comparison of chlorophyll fluorescence measurement, post-chilling growth and visible symptoms of injury in Zea mays. Plant Physiology 72, 241–247.
CrossRef | CAS | open url image1

Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1997) Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. Journal of Experimental Botany 48, 1105–1113.
CrossRef | CAS | open url image1

Holá D, Langrova KM, Kocova M, Rothova O (2003) Photosynthetic parameters of maize (Zea mays L.) inbred lines and F1 hybrids: their different response to, and recovery from rapid or gradual onset of low-temperature stress. Photosynthetica 41, 429–442.
CrossRef | open url image1

Horvàth E, Janda T, Szalai G, Paldi E (2002) In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Science 163, 1129–1135.
CrossRef | open url image1

Horváth E, Pál M, Szalai G, Páldi E, Janda T (2007) Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biologia Plantarum 51, 480–487.
CrossRef | open url image1

Hund A, Fracheboud Y, Soldati A, Frascaroli E, Salvi S, Stamp P (2004) QTL controlling root and shoot traits of maize seedlings under cold stress. Theoretical and Applied Genetics 109, 618–629.
CrossRef | CAS | PubMed | open url image1

Hund A, Frascaroli E, Leipner J, Jompuk C, Stamp P, Fracheboud Y (2005) Cold tolerance of the photosynthetic apparatus: pleiotropic relationship between photosynthetic performance and specific leaf area of maize seedlings. Molecular Breeding 16, 321–331.
CrossRef | CAS | open url image1

Hund A, Richner W, Soldati A, Fracheboud Y, Stamp P (2007) Root morphology and photosynthetic performance of maize inbred lines at low temperature. European Journal of Agronomy 27, 52–61.
CrossRef | open url image1

Janda T, Szalai G, Szalai J, Kissimon E, Paldi C, Marton ZS (1994) Role of irradiance in the chilling injury of young maize plants studied by chlorophyll fluorescence induction measurements. Photosynthetica 30, 293–299.
CAS |
open url image1

Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effect of chilling injury in maize (Zea mays L.) plants. Planta 208, 175–180.
CrossRef | CAS | open url image1

Janowiak F, Dörffling K (1996) Chilling of maize seedlings: changes in water status and abscisic acid content in ten genotypes differing in chilling tolerance. Journal of Plant Physiology 147, 582–588.
CAS |
open url image1

Janowiak F, Luck E, Dörffling K (2003) Chilling tolerance of maize seedlings in the field during cold periods in spring is related to chilling-induced increase in abscisic acid level. Journal of Agronomy and Crop Science 189, 156–161.
CrossRef | CAS | open url image1

Janowiak F, Markowski A (1994) Changes in leaf water relations and injuries in maize seedlings induced by different chilling conditions. Journal of Agronomy and Crop Science 172, 19–28.
CrossRef | open url image1

Janowiak F, Maas B, Dörffling K (2002) Importance of abscisic acid for chilling tolerance of maize seedlings. Journal of Plant Physiology 159, 635–643.
CrossRef | CAS | open url image1

Jompuk C, Fracheboud Y, Stamp P, Leipner J (2005) Mapping of quantitative trait loci associated with chilling tolerance in maize (Zea mays L.) seedlings grown under field conditions. Journal of Experimental Botany 56, 1153–1163.
CrossRef | CAS | PubMed | open url image1

Kaspar TC, Bland WL (1992) Soil temperature and root growth. Soil Science 154, 290–299.
CrossRef | open url image1

Khorshidi M, Nojavan AM (2006) The effect of abscisic acid and CaCl2 on the activities of antioxidant enzymes under cold stress in maize seedling under dark. Pakistan Journal of Biological Sciences 9, 54–59.
CrossRef | CAS | open url image1

Kiel C, Stamp P (1992) Internal root anatomy of maize seedlings (Zea mays L.) as influenced by temperature and genotype. Annals of Botany 70, 125–128. open url image1

Kingston-Smith AH, Foyer CH (2000a) Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to parquet or low temperatures. Journal of Experimental Botany 51, 123–130.
CrossRef | CAS | PubMed | open url image1

Kingston-Smith AH, Foyer CH (2000b) Over expression of Mn-superoxide dismutase in maize leaves leads to increased monodehydroascorbate reductase, dehydroascorbate reductase and glutathione reductase activities. Journal of Experimental Botany 51, 1867–1877.
CrossRef | CAS | PubMed | open url image1

Kingston-Smith AH, Harbinson J, Williams J, Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiology 114, 1039–1046.
CAS | PubMed |
open url image1

Kocsy G, Brunner M, Rüegsegger A, Stamp P, Brunold C (1996) Glutathione synthesis in maize genotypes with different sensitivity to chilling. Planta 198, 365–370.
CrossRef | CAS | open url image1

Kocsy G, Von BP, Rüegsegger A, Szalai G, Galiba G, Brunold C (2001) Increasing the glutathione content in a chilling-sensitive maize genotype using safeners increased protection against chilling-induced injury. Plant Physiology 127, 1147–1156.
CrossRef | CAS | PubMed | open url image1

Kocsy G, Von BP, Suter M, Rüegsegger A, Galli U, Szalai G, Galiba G, Brunold C (2000) Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211, 528–536.
CrossRef | CAS | PubMed | open url image1

Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant, Cell & Environment 23, 337–350.
CrossRef | CAS | open url image1

Landi P, Albrecht B, Giuliani MM, Sanguineti MC (1998) Seedling characteristics in hydroponic culture and field performance of maize genotypes with different resistance to root lodging. Maydica 43, 111–116. open url image1

Lee CB, Hayashi H, Moon BY (1997) Stabilization by glycinebetaine of photosynthetic oxygen evolution by thylakoid membranes from Synechococcus PCC7002. Molecular Cell 7, 296–299.
CAS |
open url image1

Lee TM, Lur HS, Chu C (1993) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings. Endogenous abscisic acid levels. Plant, Cell & Environment 16, 481–490.
CrossRef | CAS | open url image1

Lee EA, Staebler MA, Tollenaar M (2002) Genetic variation in physiological discriminators for cold tolerance – early autotrophic phase of maize development. Crop Science 42, 1919–1929. open url image1

Leegood RC, Edwards GE (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In ‘Advances in photosynthesis. Vol. 5. Photosynthesis and the environment’. (Ed. NR Baker) pp. 191–221. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Leipner J, Fracheboud Y, Stamp P (1997) Acclimation by suboptimal growth temperature diminishes photo-oxidative damage in maize leaves. Plant, Cell & Environment 20, 366–372.
CrossRef | CAS | open url image1

Leipner J, Fracheboud Y, Stamp P (1999) Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. Environmental and Experimental Botany 42, 129–139.
CrossRef | CAS | open url image1

Leipner J, Stamp P (2009) Chilling stress in maize seedlings. In ‘Handbook of maize: its biology’. (Eds LJ Bennetzen, SC Hake) pp. 291–310. (Springer: New York)

Li PH, Chen WP, Jian L, Xin Z (1997) Abscisic acid-induced chilling tolerance in maize. In ‘Plant cold hardiness. Molecular biology, biochemistry and physiology’. (Eds PH Li, THH Chen) pp. 215–223. (Plenum Press: New York, London)

Long SP (1983) C4 photosynthesis at low temperatures. Plant, Cell & Environment 6, 345–363.
CAS |
open url image1

Long SP, East TM, Baker NR (1983) Chilling damage to photosynthesis in young Zea mays. Journal of Experimental Botany 34, 177–188.
CrossRef | open url image1

Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annual Review of Plant Physiology and Plant Molecular Biology 45, 633–662.
CrossRef | CAS | open url image1

MacKay AD, Barber SA (1984) Soil temperature effects on root-growth and phosphorus uptake by corn. Soil Science Society of America Journal 48, 818–823.
CAS |
open url image1

Markhart AH (1984) Amelioration of chilling-induced water stress by abscisic acid-induced changes in root hydraulic conductance. Plant Physiology 74, 81–83.
CrossRef | CAS | PubMed | open url image1

Marocco A, Lorenzoni C, Fracheboud Y (2005) Chilling stress in maize. Maydica 50, 571–580. open url image1

Matzner S, Comstock J (2001) The temperature dependence of shoot hydraulic resistance: implications for stomatal behaviour and hydraulic limitation. Plant, Cell & Environment 24, 1299–1307.
CrossRef | open url image1

McMichael BL, Burke JJ (2003) Genetic variability for early season root system development. In ‘National Cotton Council Beltwide Cotton Conference’. p. 1748. (USDA)

McWilliam JR, Kramer PJ, Musser RL (1982) Temperature-induced water stress in chilling-sensitive plants. Australian Journal of Plant Physiology 9, 343–352. open url image1

Miedema P (1982) The effects of low temperature on Zea mays. Advances in Agronomy 35, 93–128.
CrossRef | open url image1

Miedema P, Post J, Groot P (1987) The effect of low temperature on seedling growth of maize genotypes. Agric. Research Reports 926. pp. 343–406. (Pudoc: Wageningen, and Cold Spring Harbor: New York)

Monika M, Janda T, Horvath E, Paldi E, Szalai G (2001) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Science 162, 569–574. open url image1

Muldoon DK, Wheeler JL, Pearson CJ (1984) Growth mineral composition and digestibility of maize, sorghum and barnyard millets at different temperatures. Australian Journal of Agricultural Research 35, 367–378.
CrossRef | open url image1

Nayyar H, Bains T, Kumar S (2005) Low temperature induced floral abortion in chickpea: Relationship with abscisic acid and cryoprotectants in reproductive organs. Environmental and Experimental Botany 53, 39–47.
CrossRef | CAS | open url image1

Nie GY, Long SP, Baker NR (1992) The effects of development at sub-optimal growth temperature on photosynthetic capacity and susceptibility to chilling-dependent photoinhibition in Zea mays L. Physiologia Plantarum 85, 554–560.
CrossRef | CAS | open url image1

Nie GY, Robertson EJ, Fryer MJ, Leech RM, Baker NR (1995) Response of the photosynthetic apparatus in maize leaves grown at low temperature on transfer to normal temperature. Plant, Cell & Environment 18, 1–12.
CrossRef | CAS | open url image1

Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipids. Annual Review of Plant Physiology and Plant Molecular Biology 47, 541–568.
CrossRef | CAS | PubMed | open url image1

Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono M, Kwbo A, Kanna M, Ioki M, Kamada H, Saji H (2005) Salicylic acid accumulation under O3 exposure is regulated by ethylene in tobacco plants. Plant & Cell Physiology 46, 1062–1072.
CrossRef | CAS | PubMed | open url image1

Pan WL, Jackson WA, Moll RH (1985) Nitrate uptake and partitioning by corn (Zea mays L.) root systems and associated morphological differences among genotypes and stages of root development. Journal of Experimental Botany 36, 1341–1351.
CrossRef | open url image1

Parikova GO, Ciamporova M, Tamas L, Trginova I, Luxova M (1996) Cold-induced changes in protein patterns and ultrastructure of root cells of maize seedling. Biologia 51, 449–456. open url image1

Pastori GM, Foyer CH, Mullineaux PM (2000) Low temperature induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. Journal of Experimental Botany 51, 107–113.
CrossRef | CAS | PubMed | open url image1

Peng Z, Lu Q, Verma DP (1996) Reciprocal regulation of delta 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Molecular & General Genetics 253, 334–341.
CrossRef | CAS | open url image1

Pietrini F, Ianneli MA, Battistelli A, Moscatello S, Loreto F, Massacci A (1999) Effects on photosynthesis, carbohydrate accumulation and re-growth increase in maize genotypes with different sensitivity to low temperature. Australian Journal of Plant Physiology 26, 367–373. open url image1

Pimentel C, Davey PA, Juvik JA, Long SP (2005) Gene loci in maize influencing susceptibility to chilling dependent photoinhibition of photosynthesis. Photosynthesis Research 85, 319–326.
CrossRef | CAS | PubMed | open url image1

Prasad TK (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. The Plant Journal 10, 1017–1026.
CrossRef | CAS | open url image1

Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergence maize seedlings. Plant Physiology 114, 1369–1376.
CAS | PubMed |
open url image1

Prasad TK, Anderson MD, Stewart CR (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology 105, 619–627.
CAS | PubMed |
open url image1

Presterl T, Ouzunova M, Schmidt W, Möller EM, Röber FK, Knaak C, Ernst K, Westhoff P, Geiger HH (2007) Quantitative trait loci for early plant vigour of maize grown in chilly environments. Theoretical and Applied Genetics 114, 1059–1070.
CrossRef | PubMed | open url image1

Pritchard J, Barlow PW, Adams JS, Tomos AD (1990) Biophysics of the inhibition of the growth of maize roots by lowered temperature. Plant Physiology 93, 222–230.
CrossRef | PubMed | open url image1

Purvis AC, Shewfelt RL (1993) Does alternative pathway ameliorate chilling injury in sensitive plant tissues. Plant Physiology 88, 712–718.
CrossRef | CAS | open url image1

Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Science 166, 141–149.
CrossRef | CAS | open url image1

Ramakrishna A, Tam HM, Wani SP, Long TD (2006) Effect of mulch on soil temperature, moisture, weed infestation and yield of groundnut in northern Vietnam. Field Crops Research 95, 115–125.
CrossRef | open url image1

Revilla P, Butron A, Malvar RA, Ordas A (1999) Relationships among kernel weight, early vigor, and growth in maize. Crop Science 39, 654–658. open url image1

Revilla P, Malvar RA, Cartea ME, Ordas A (1998) Identifying open pollinated populations of field corn as sources of cold tolerance for improving sweet corn. Euphytica 101, 239–247.
CrossRef | open url image1

Revilla P, Malvar RA, Careta ME, Butrón A, Ordás A (2000) Inheritance of cold tolerance at emergence and during early season growth in maize. Crop Science 40, 1579–1585. open url image1

Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 44, 357–384.
CrossRef | CAS | open url image1

Rhodes D, Rich PJ, Brunk DG, Ju GC, Rhodes JC, Pauly MH, Hansen LA (1989) Development of two isogenic sweet corn hybrids differing for glycinebetaine content. Plant Physiology 91, 1112–1121.
CrossRef | CAS | PubMed | open url image1

Rhodes D, Rich PJ, Myers AC, Reuter CC, Jamieson GC (1987) Determination of betaines by fast atom bombardment mass spectrometry: identification of glycinebetaine deficient genotypes of Zea mays. Plant Physiology 84, 781–788.
CrossRef | CAS | PubMed | open url image1

Richner W, Kiel C, Stamp P (1997) Is seedling root morphology predictive of seasonal accumulation of shoot dry matter in maize. Crop Science 37, 1237–1241. open url image1

Richner W, Soldati A, Stamp P (1996) Shoot-to-root relations in field-grown maize seedlings. Agronomy Journal 88, 56–61. open url image1

Ristic Z, Yang G, Sterzinger A, Zhang L (1998) Higher chilling tolerance in maize is not always related to the ability for greater and faster abscisic acid accumulation. Journal of Plant Physiology 153, 154–162.
CAS |
open url image1

Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents – proline, betaine, and trehalose – on membrane phospholipids. Archives of Biochemistry and Biophysics 245, 134–143.
CrossRef | CAS | PubMed | open url image1

Sakamoto A, Murata N (2002) The role of glycinebetaine in the protection of plants from stress clues from transgenic plants. Plant, Cell & Environment 25, 163–171.
CrossRef | CAS | PubMed | open url image1

Saradhi PP, Alia AS, Prasad KVSK (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochemical and Biophysical Research Communications 209, 1–5.
CrossRef | CAS | PubMed | open url image1

Saropulos AS, Drennan DSH (2007) Ultrastructural alterations in mesophyll and bundle sheath chloroplasts of two maize cultivars in response to chilling at high irradiance. Biologia Plantarum 51, 690–698.
CrossRef | open url image1

Serraj R, Sinclair TR (2002) Osmolyte accumulation can it really help increase crop yield under drought conditions. Plant, Cell & Environment 25, 333–341.
CrossRef | PubMed | open url image1

Shabala S, Shabala L (2002) Kinetics of net H+, Ca2+, K+, Na+, NH4+, and Cl- fluxes associated with post-chilling recovery of plasma membrane transporters in Zea mays leaf and root tissues. Physiologia Plantarum 114, 47–56.
CrossRef | CAS | PubMed | open url image1

Shou H, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proceedings of the National Academy of Sciences of the United States of America 101, 3298–3303.
CrossRef | CAS | PubMed | open url image1

Smirnoff N, Cumbes QJ (1989) Hydroxyl radicle scavenging activity of compatible solutes. Phytochemistry 28, 1057–1060.
CrossRef | CAS | open url image1

Sowiński P, Rudzinska-Langwald A, Adamczyk J, Kubica I, Fronk J (2005) Recovery of maize seedling growth, development and photosynthetic efficiency after initial growth at low temperature. Journal of Plant Physiology 162, 67–80.
CrossRef | PubMed | open url image1

Sowiński P, Rudzińska-Langwald A, Kobus P (2003) Changes in plasmodesmata frequency in vascular bundles of maize seedling leaf induced by growth at sub-optimal temperatures in relation to photosynthesis and assimilate export. Environmental and Experimental Botany 50, 183–196.
CrossRef | open url image1

Stamp P (1984) Chilling tolerance of young plants demonstrated on the example of maize (Zea mays L.). In ‘Advances in agriculture and crop science Vol. 7’. (Ed. G Geisler) pp. 1–84. (Paul Parey: Berlin)

Stamp P (1986) Chilling stress in maize. In ‘Breeding of silage maize. Proceedings of Eucarpia Workshop’. (Eds O Dolstra, P Miedema) pp. 43–50. (Pudoc: Wageningen, The Netherlands)

Stamp P, Feil B, Schortemeyer M, Richner W (1997) Responses of roots to low temperatures and nitrogen forms. In ‘Plant roots from cells to systems’. (Ed. HM Anderson) pp. 143–154. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Steffens D (1986) Root system and potassium exploitation. In ‘Nutrient balances and the need for potassium. Proceedings of Congress’. pp. 107–188. (International Potash Institute: Berne)

Steudle E (2000) Water uptake by roots: effects of water deficit. Journal of Experimental Botany 51, 1531–1542.
CrossRef | CAS | PubMed | open url image1

Stewart CR, Martin BA, Reding L, Cenvick S (1990) Seedling growth, mitochondrial characteristics, and alternative respiratory capacity of corn genotypes differing in cold tolerance. Plant Physiology 92, 761–766.
CrossRef | CAS | PubMed | open url image1

Stone PJ, Sorensen IB, Jamieson PD (1999) Effect of soil temperature on phenology, canopy development, biomass and yield of maize in a cool-temperature climate. Field Crops Research 63, 169–178.
CrossRef | open url image1

Subedi KD, Ma BL (2005) Seed priming does not improve corn yield in a humid temperate environment. Agronomy Journal 97, 211–218. open url image1

Taylor AG, Allen PS, Bennett MA, Bradford KJ, Burris JS, Misra MK (1998) Seed enhancements. Seed Science Research 8, 245–256.
CrossRef | open url image1

Thornley JHM, Johnson IR (1990) ‘Plant and crop modelling: a mathematical approach to plant and crop physiology.’ (Oxford Science Publications: Oxford, UK)

Tollenaar M, Daymard TB, Hunter RB (1979) Effect of temperature on rate of leaf appearance and flowering date in maize. Crop Science 19, 363–366. open url image1

Troyer AF (1999) Background of US hybrid corn. Crop Science 39, 601–626. open url image1

Tuberosa R, Frascaroli E, Salvi S, Sanguineti MC, Conti S, Landi P (2008) QTLS for tolerance to abiotic stresses in maize: Present status and prospects. Maydica 53, 559–569. open url image1

Van Breusegem F, Slooten L, Stassart J-M, Moens T, Botterman J, Van Montagu M, Inzé D (1999) Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant & Cell Physiology 40, 515–523.
CAS | PubMed |
open url image1

Verheul MJ, Hasselt PRV, Stamp P (1995) Comparison of maize inbred lines differing in low temperature tolerance effect of acclimation at suboptimal temperature on chloroplast functioning. Annals of Botany 76, 7–14.
CrossRef | CAS | open url image1

Verheul MJ, Picatto C, Stamp P (1996) Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field. European Journal of Agronomy 5, 31–43.
CrossRef | open url image1

Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
CrossRef | open url image1

Wahid A, Sehar S, Perveen M, Gelani S, Basra SMA, Farooq M (2008) Seed pretreatment with hydrogen peroxide improves heat tolerance in maize at germination and seedling growth stages. Seed Science and Technology 36, 633–645. open url image1

Warrington IJ, Kanemasu ET (1983a) Corn growth response to temperature and photoperiod I. Seedling emergence, tassel initiation, and anthesis. Agronomy Journal 75, 749–754. open url image1

Warrington IJ, Kanemasu ET (1983b) Corn growth response to temperature and photoperiod II. Leaf-initiation and leaf-appearance rates. Agronomy Journal 75, 755–761. open url image1

Wise RR (1995) Chilling enhanced photooxidation the production, action and study of reactive oxygen species produced during chilling in the light. Photosynthesis Research 45, 79–97.
CrossRef | CAS | open url image1

Wise RR, Cook WB (1998) Development of ultrastructural damage to choloroplast in a plastoquinone-deficient mutant of maize. Environmental and Experimental Botany 40, 221–228.
CrossRef | open url image1

Wolfe J (1978) Chilling injury in plants the role of membrane lipid fluidity. Plant, Cell & Environment 1, 241–247.
CrossRef | open url image1

Xin Z, Li PH (1992) Abscisic acid-induced chilling tolerance in maize suspension-cultured cells. Plant Physiology 99, 707–711.
CrossRef | CAS | PubMed | open url image1

Xing W, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress is Arabidopsis thaliana. Environmental and Experimental Botany 46, 21–28.
CrossRef | CAS | PubMed | open url image1

Yalpani N, Enyedi AJ, Leon J, Raskin I (1994) Ultraviolet light and ozone stimulates accumulation of salicylic acid, pathogen-related proteins and virus resistance in tobacco. Planta 193, 372–376.
CrossRef | CAS | open url image1








Rent Article (via Deepdyve) Export Citation Cited By (30)