Maize plants can enter a standby mode to cope with chilling stress

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  Riva Roveda, Laëtitia ^a,b,d   Escale, Brigitte ^a   Giauffret, Catherine ^b,c   Périlleux, Claire ^d  

^a Service Génétique   (France)

^b UNIV LILLE   (France)

^c Inst Natl de la Rech Agronomique   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Cold tolerance; Leaf growth; Maize (Zea mays); Photoprotection

Indexed keywords

ADAPTATION; COLD; GENETICS; MAIZE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT BREEDING; PLANT LEAF;

ADAPTATION, PHYSIOLOGICAL; COLD TEMPERATURE; PLANT BREEDING; PLANT LEAVES; STRESS, PHYSIOLOGICAL; ZEA MAYS;

EID: 84992065901     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-016-0909-y     Document Type: Article

References (55)

1. Rebourg C, Chastanet M, Gouesnard B, Welcker C, Dubreuil P, Charcosset A. Maize introduction into Europe: the history reviewed in the light of molecular data. Theor Appl Genet. 2003;106:895-903.
2. Doebley J, Wendel JD, Smith JSC, Stuber CW, Goodman MM. The origin of cornbelt maize: the isozyme evidence. Econ Bot. 1988;42:120-31.
3. Tenaillon MI, Charcosset A. A European perspective on maize history. C R Biol. 2011;334:221-8.
4. Rodríguez VM, Butron A, Sandoya G, Ordas A, Revilla P. Combining maize base germplasm for cold tolerance breeding. Crop Sci. 2007;47:1467-74.
5. Barrière Y, Alber D, Dolstra O, Lapierre C, Motto M, Ordas A, et al. Past and prospects of forage maize breeding in Europe. II. History, germplasm evolution and correlative agronomic changes. Maydica. 2006;51:435-49.
6. Lorgeou J, Prioul JL. Agrophysiology: light interception, crop photosynthesis, mineral nutrition and crop managing. In: Prioul JL, Thévenot C, Molnar T, editors. Advances in Maize. London: Society of Experimental Biology; 2011. p. 393-410.
7. Marocco A, Lorenzoni C, Fracheboud Y. Chilling stress in maize. Maydica. 2005;50:571-80.
8. Leipner J, Stamp P. Chilling stress in maize seedlings. In: Bennetzen JL, Hake SC, editors. Handbook of Maize. New York: Springer; 2009. p. 291-310.
9. Miedema P. The effects of low temperature on Zea mays. Adv Agron. 1982;35:93-128.
10. Louarn G, Chenu K, Fournier C, Andrieu B, Giauffret C. Relative contributions of light interception and radiation use efficiency to the reduction of maize productivity under cold temperatures. Funct Plant Biol. 2008;35:885-99.
11. Giauffret C, Foyer CH. Effects of chilling temperatures on maize growth and biomass production. In: Prioul JL, Thévenot C, Molnar T, editors. Advances in Maize. London: Society of Experimental Biology; 2011. p. 347-72.
12. Revilla P, Malvar RA, Cartea ME, Butron A, Ordas A. Inheritance of cold tolerance at emergence and during early season growth in maize. Crop Sci. 2000;40:1579-85.
13. Leipner J, Jompuk C, Camp KH, Stamp P, Fracheboud Y. QTL studies reveal little relevance of chilling-related seedling traits for yield in maize. Theor Appl Genet. 2008;116:555-62.
14. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, et al. The developmental dynamics of the maize leaf transcriptome. Nat Genet. 2010;42:1060-7.
15. Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS. Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol. 2007;143:1429-38.
16. Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, et al. Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One. 2011;6:e22132.
17. Chinnusamy V, Zhu J. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12:444-51.
18. Miura K. ICE1, a transcription factor involved in cold signaling and tolerance. In: Imai R, Yoshida M, Matsumoto N, editors. Plant and microbe adaptations to cold in a changing world. New York: Springer; 2013. p. 189-95.
19. Sylvester AW, Smith LG. Cell biology of maize leaf development. In: Bennetzen J, Hake S, editors. Handbook of Maize: its biology. New York: Springer; 2009. p. 179-203.
20. Parent B, Turc O, Gibon Y, Stitt M, Tardieu F. Modelling temperature-compensated physiological rates, based on the co-ordination of responses to temperature of developmental processes. J Exp Bot. 2010;61:2057-69.
21. Louarn G, Andrieu B, Giauffret C. A size-mediated effect can compensate for transient chilling stress affecting maize (Zea mays) leaf extension. New Phytol. 2010;187:106-18.
22. Caffarri S, Frigerio S, Olivieri E, Righetti PG, Bassi R. Differential accumulation of Lhcb gene products in thylakoid membranes of Zea mays plants grown under contrasting light and temperature conditions. Proteomics. 2005;5:758-68.
23. 2 content and antioxidants in maize (Zea mays) grown at sub-optimal temperatures. Plant Cell Environ. 1999;22:1071-83.
24. Kutík J, Holá D, Kočová M, Rothová O, Haisel D, Wilhelmová N, et al. Ultrastructure and dimensions of chloroplasts in leaves of three maize (Zea mays L.) inbred lines and their F1 hybrids grown under moderate chilling stress. Photosynthetica. 2004;42:447-55.
25. Baker NR, Nie GY. Chilling sensitivity of photosynthesis in maize. In: Bajaj YPS, editor. Biotechnology in agriculture and forestry 25 - Maize. Berlin: Springer; 1994. p. 465-81.
26. Fracheboud Y, Haldimann P, Leipner J, Stamp P. Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). J Exp Bot. 1999;50:1533-40.
27. Baker NR. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol. 2008;59:89-113.
28. Bhosale SU, Rymen B, Beemster GTS, Melchinger AE, Reif JC. Chilling tolerance of central european maize lines and their factorial crosses. Ann Bot. 2007;100:1315-21.
29. Strigens A, Freitag NM, Gilbert X, Grieder C, Riedelsheimer C, Schrag TA, et al. Association mapping for chilling tolerance in elite Flint and Dent maize inbred lines evaluated in growth chamber and field experiments. Plant Cell Environ. 2013;36:1871-87.
30. Lejeune P, Bernier G. Effect of environment on the early steps of ear initiation in maize (Zea mays L.). Plant Cell Environ. 1996;19:217-24.
31. Hendrickson L, Furbank RT, Chow WS. A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res. 2004;82:73-81.
32. Böddi B, Loudeche R, Franck F. Delayed chlorophyll accumulation and pigment photodestruction in the epicotyls of dark-grown pea (Pisum sativum). Physiol Plant. 2005;125:365-72.
33. Pietrini F, Iannelli MA, Battistelli A, Moscatello S, Loreto F, Massacci A. Effects on photosynthesis, carbohydrate accumulation and regrowth induced by temperature increase in maize genotypes with different sensitivity to low temperature. Aust J Plant Physiol. 1999;26:367-73.
34. Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, et al. Genome-wide atlas of transcription during maize development. Plant J. 2011;66:553-63.
35. Manoli A, Sturaro A, Trevisan S, Quaggiotti S, Nonis A. Evaluation of candidate reference genes for qPCR in maize. J Plant Physiol. 2012;169:807-15.
36. Pabinger S, Rödiger S, Kriegner A, Vierlinger K, Weinhäusel A. A survey of tools for the analysis of quantitative PCR (qPCR) data. BDQ. 2014;1:23-33.
37. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30:e36.
38. Murchie EH, Lawson T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot. 2013;64:3983-98.
39. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, et al. Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol. 2004;45:1042-52.
40. Muller B, Bourdais G, Reidy B, Bencivenni C, Massonneau A, Condamine P, et al. Association of specific expansins with growth in maize leaves is maintained under environmental, genetic, and developmental sources of variation. Plant Physiol. 2007;143:278-90.
41. Tanaka R, Oster U, Kruse E, Rüdiger W, Grimm B. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol. 1999;120:695-704.
42. Sánchez B, Rasmussen A, Porter JR. Temperatures and the growth and development of maize and rice: a review. Global Chang Biol. 2014;20:408-17.
43. Goh H-H, Sloan J, Dorca-Fornell C, Fleming A. Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol. 2012;159:1759-70.
44. Bauerfeind MA, Winkelmann T, Franken P, Druege U. Transcriptome, carbohydrate, and phytohormone analysis of Petunia hybrida reveals a complex disturbance of plant functional integrity under mild chilling stress. Front Plant Sci. 2015;6:583.
45. Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, et al. Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol. 2015;167:800-16.
46. Long SP, Spence AK. Toward cool C4 crops. Annu Rev Plant Biol. 2013;64:701-22.
47. Naidu SL, Long SP. Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus x giganteus: an in vivo analysis. Planta. 2004;220:145-55.
48. Massad RS, Tuzet A, Bethenod O. The effect of temperature on C4-type leaf photosynthesis parameters. Plant Cell Environ. 2007;30:1191-204.
49. Koch KE. Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:509-40.
50. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell. 2007;19:1403-14.
51. Genty B, Briantais J-M, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subjects. 1989;990:87-92.
52. Leipner J, Fracheboud Y, Stamp P. Acclimation by suboptimal growth temperature diminishes photooxidative damage in maize leaves. Plant Cell Environ. 1997;20:366-72.
53. Bratt CE, Arvidsson PO, Carlsson M, Åkerlund HE. Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res. 1995;45:169-75.
54. Nie GY, Baker NR. Modifications to thylakoid composition during development of maize leaves at low growth temperatures. Plant Physiol. 1991;95:184-91.
55. Verheul MJ, Picatto C, Stamp P. Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field. Eur J Agron. 1996;5:31-43.