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Background  The cucumber is one of the most important vegetables worldwide and is used as a research model for study of phloem transport, sex determination and temperature-photoperiod physiology. The shoot apex is the most important plant tissue in which the cell fate and organ meristems have been determined. In this study, a series of whole-genome small RNA, degradome and transcriptome analyses were performed on cucumber shoot apical tissues treated with high vs. low temperature and long vs. short photoperiod.    Results  A total of 164 known miRNAs derived from 68 families and 203 novel miRNAs from 182 families were identified. Their 4611 targets were predicted using psRobot and TargetFinder, amongst which 349 were validated by degradome sequencing. Fourteen targets of six miRNAs were differentially expressed between the treatments. A total of eight known and 16 novel miRNAs were affected by temperature and photoperiod. Functional annotations revealed that “Plant hormone signal transduction” pathway was significantly over-represented in the miRNA targets. The miR156/157/ SBP-Boxes  and novel-mir153/ ethylene-responsive transcription factor/senescence-related protein/aminotransferase/acyl-CoA thioesterase  are the two most credible miRNA/targets combinations modulating the plant’s responsive processes to the temperature-photoperiod changes. Moreover, the newly evolved, cucumber-specific novel miRNA (novel-mir153) was found to target 2087 mRNAs by prediction and has 232 targets proven by degradome analysis, accounting for 45.26–58.88% of the total miRNA targets in this plant. This is the largest sum of genes targeted by a single miRNA to the best of our knowledge.    Conclusions  These results contribute to a better understanding of the miRNAs mediating plant adaptation to combinations of temperature and photoperiod and sheds light on the recent evolution of new miRNAs in cucumber.    Electronic supplementary material  The online version of this article (10.1186/s12864-018-5204-x) contains supplementary material, which is available to authorized users.

MicroRNAs and their targets in cucumber shoot apices in response to temperature and photoperiod