Molecular foundations of chilling-tolerance of modern maize

Abstract

BackgroundRecent progress in selective breeding of maize (Zea mays L.) towards adaptation to temperate climate has allowed the production of inbred lines withstanding cold springs with temperatures below 8 °C or even close to 0 °C, indicating that despite its tropical origins maize is not inherently cold-sensitive.ResultsHere we studied the acclimatory response of three maize inbred lines of contrasting cold-sensitivity selected basing on multi-year routine field data. The field observations were confirmed in the growth chamber. Under controlled conditions the damage to the photosynthetic apparatus due to severe cold treatment was the least in the cold-tolerant line provided that it had been subjected to prior moderate chilling, i.e., acclimation. The cold-sensitive lines performed equally poorly with or without acclimation. To uncover the molecular basis of the attained cold-acclimatability we performed comparative transcriptome profiling of the response of the lines to the cold during acclimation phase by means of microarrays with a statistical and bioinformatic data analysis.ConclusionsThe analyses indicated three mechanisms likely responsible for the cold-tolerance: acclimation-dependent modification of the photosynthetic apparatus, cell wall properties, and developmental processes. Those conclusions supported the observed acclimation of photosynthesis to severe cold at moderate chilling and were further confirmed by experimentally showing specific modification of cell wall properties and repression of selected miRNA species, general regulators of development, in the cold-tolerant line subjected to cold stress.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2453-4) contains supplementary material, which is available to authorized users.

Global analysis of gene expression in maize leaves treated with low temperature. II. Combined effect of severe cold (8 °C) and circadian rhythm

“…3 h. This response was not unique to the CM109 line studied here. Also in other maize inbreds studied by us earlier the transcript levels of the clock genes showed similar changes upon treatment with severe (Sobkowiak et al 2014) or moderate cold (Sobkowiak et al 2016;Jończyk et al unpublished data) when analyzed at a single time point (Fig. 6).…”

“…We have previously documented excellent correspondence of the microarray data with RNA quantitation obtained by RT-qPCR (Trzcinska-Danielewicz et al 2009;Sobkowiak et al 2014Sobkowiak et al , 2016.…”

“…Only the metabolic pathways modified specifically under severe cold stress identified by the meta-analysis of published microarray projects concerning severe cold (<10 °C; Sobkowiak et al 2014 and this work), moderate chilling (ca. 14 °C; Sobkowiak et al 2016) and fungal attack (Doehlemann et al 2008) stresses will be discussed here.…”

“…Further RNA extraction, purification, amplification, Cy3 and Cy5 dye coupling and hybridization to microarrays were done following procedures described by the microarray manufacturer with minor modifications (Sobkowiak et al 2016). Samples were hybridized in the reference design, i.e., each sample was paired with the time-zero sample from a given biological replication.…”

“…At the biochemical and physiological levels, several processes have been identified as key contributors to this sensitivity. They include damage to the photosynthetic apparatus affecting redox balance and enhancing production of reactive oxygen species (Foyer et al 2002); reduced activity of enzymes of the dark phase of photosynthesis (Leipner and Stamp 2009) and compromised phloem loading (Sowiński et al 2001), together affecting the carbohydrate status of the leaf (Sowiński et al 1999;Marocco et al 2005); alteration of secondary metabolism (Christie et al 1994); modification of the cell wall (Sobkowiak et al 2016;Bilska-Kos et al 2017); and water deficit (Janowiak and Markowski 1994).…”