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.
Maize is a cold-sensitive species, but selective breeding programs have recently succeeded in producing plants strikingly well adapted to the cold springs of a temperate climate, showing the potential for improved cold tolerance. The aim of the present study was to determine whether the adaptation of some inbred lines to spring chills is due to their increased true cold tolerance or whether it only represents an avoidance mechanism, which was the sole mode of adaptation during early stages of agricultural dispersal of maize towards higher latitudes. By characterizing numerous physiological features of several lines of different cold sensitivity, we show that a combination of both avoidance and tolerance is involved. A novel avoidance mechanism was found that favored unhindered development of the photosynthetic apparatus through protection of the shoot apex below soil level due to a shortened mesocotyl. It seems to be mediated by increased seedling photosensitivity at early growth stages. True tolerance involved improved protection of the cell membrane against cold injury at temperatures close to 0 °C and stimulation of light-induced processes (accumulation of anthocyanins, carotenoids, and chlorophyll, proper development of chloroplasts) at temperatures in the range of 10–14 °C, likely also related to the increased photosensitivity and mediated by gibberellin signaling.
C(4) photosynthesis involves cell-to-cell exchange of photosynthetic intermediates between the Kranz mesophyll (KMS) and bundle sheath (BS) cells. This was believed to occur by simple diffusion through plentiful plasmodesmatal (PD) connections between these cell types. The model of C(4) intermediates' transport was elaborated over 30 years ago and was based on experimental data derived from measurements at the time. The model assumed that plasmodesmata occupied about 3% of the interface between the KMS and BS cells and that the plasmodesmata structure did not restrict metabolite movement. Recent advances in the knowledge of plasmodesmatal structure put these assumptions into doubt, so a new model is presented here taking the new anatomical details into account. If one assumes simple diffusion as the sole driving force, then calculations based on the experimental data obtained for C(4) grasses show that the gradients expected of C(4) intermediates between KMS and BS cells are about three orders of magnitude higher than experimentally estimated. In addition, if one takes into account that the plasmodesmata microchannel diameter might constrict the movement of C(4) intermediates of comparable Stokes' radii, the differences in concentration of photosynthetic intermediates between KMS and BS cells should be further increased. We believe that simple diffusion-driven transport of C(4) intermediates between KMS and BS cells through the plasmodesmatal microchannels is not adequate to explain the C(4) metabolite exchange during C(4) photosynthesis. Alternative mechanisms are proposed, involving the participation of desmotubule and/or active mechanisms as either apoplasmic or vesicular transport.
The chloroplast peripheral reticulum (PR) is a structure of unknown function. Some authors postulated that it is a characteristic feature of C 4 plants, although it was reported from C 3 species as well. It is unknown whether the occurrence of PR follows a phylogenetic (it is found in clades containing C 4 species, regardless of the photosynthetic type) or functional (photosynthetic pathway dependent) pattern. Here, we present a phylogenetically controlled analysis of the occurrence, form and functional aspects of PR in grasses. The occurrence of the PR follows a functional and not a phylogenetic pattern. Its most elaborated form (PR type I) is a unique feature of C 4 species. Although PR was found in some of the studied C 3 grasses, it was always less developed than PR in the chloroplasts of Kranz mesophyll cells of C 4 species. The size of PR in C 4 plants was found to increase when the plants were grown under low light intensity. Additional observations, such as a negative correlation between PR size and chloroplast surface and PR occurrence in vicinity of mitochondria or plasmodesmata, suggest that PR may play some role in C 4 metabolism.
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