Chilling stress drives organ-specific transcriptional cascades and dampens diurnal oscillation in tomato

Abstract

Improving chilling tolerance in cold-sensitive crops, e.g. tomato, requires knowledge of the early molecular response to low temperature in these under-studied species. To elucidate early responding processes and regulators, we captured the transcriptional response at 30 minutes and 3 hours in the shoots and at 3 hours in the roots of tomato post-chilling from 24℃ to 4℃. We used a pre-treatment control and a concurrent ambient temperature control to reveal that majority of the differential expression between cold and ambient conditions is due to severely compressed oscillation of a large set of diurnally regulated genes in both the shoots and roots. This compression happens within 30 minutes of chilling, lasts for the duration of cold treatment, and is relieved within 3 hours of return to ambient temperatures. Our study also shows that the canonical ICE1/CAMTA-to-CBF cold response pathway is active in the shoots, but not in the roots. Chilling stress induces synthesis of known cryoprotectants (trehalose and polyamines), in a CBF-independent manner, and induction of multiple genes encoding proteins of photosystems I and II. This study provides nuanced insights into the organ-specific response in a chilling sensitive plant, as well as the genes influenced by an interaction of chilling response and the circadian clock.

Acknowledgements

We thank Prof. Rob McClung for critical discussions and comments and Nathan Deppe for technical assistance in experimental setup. This research was supported by funds from Purdue University.

Author contributions

Conceptualization, investigation, and validation were conducted by T.A. and K.V. X.W. generated the CBF1 mutant and performed gene expression analysis. F.M. designed and executed the experiments to assay resumption of clock oscillation. Formal analysis and data curation were performed by T.A. and K.V. T.A. and K.V. wrote the original draft. X.W. and F.M. participated in revision and updates. I.I. and S.P. contributed resources and methodology for photosynthetic measures. All authors contributed to reviewing and editing. K.V. is responsible for funding acquisition and project supervision.

Data Availability

All sequence and gene expression data were deposited in NCBI’s GEO database and can be retrieved with the accession number GSE226856.

Conflict of interest statement

The authors report no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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