Omics analyses in citrus reveal a possible role of RNA translation pathways and Unfolded Protein Response regulators in the tolerance to combined drought, high irradiance, and heat stress

Abstract

Environmental changes derived from global warming and human activities increase the intensity and frequency of stressful conditions for plants. Multiple abiotic factors acting simultaneously enhance stress pressure and drastically reduce plant growth, yield, and survival. Stress combination causes a specific stress situation that induces a particular plant response different to the sum of responses to the individual stresses. Here, by comparing transcriptomic and proteomic profiles to different abiotic stress combinations in two citrus genotypes, Carrizo citrange (Citrus sinensis × Poncirus trifoliata) and Cleopatra mandarin (Citrus reshni), with contrasting tolerance to different abiotic stresses, we revealed key responses to the triple combination of heat stress, high irradiance and drought. The specific transcriptomic response to this stress combination in Carrizo was directed to regulate RNA metabolic pathways and translation processes, potentially conferring an advantage with respect to Cleopatra. In addition, we found endoplasmic reticulum stress response as common to all individual and combined stress conditions in both genotypes and identified the accumulation of specific groups of heat shock proteins (HSPs), such as small HSPs and HSP70s, and regulators of the unfolded protein response, BiP2 and PDIL2-2, as possible factors involved in citrus tolerance to triple stress combination. Taken together, our findings provide new insights into the acclimation process of citrus plants to multiple stress combination, necessary for increasing crop tolerance to the changing climatic conditions.

Acknowledgements

This work was supported by Grants PID2019-104062RB-I00 and TED2021-129795B-I00 funded by MCIN/AEI/10.13039/501100011033 and by the European Union- NextGenerationEU. Funding was also obtained from Universitat Jaume I (UJI-B2022-18) and Generalitat Valenciana (CIAICO/2021/063). DB was supported by the European Union–NextGenerationEU and the Ministerio de Universidades (MGS/2021/17). S.I.Z. was supported by MCIN (RYC2020-029967- I). T.R.O. was supported by the Fundação Carlos Chagas Filho FAPERJ (E-26/204.192/2021) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES–001).

Author Contributions

D.B., S.I.Z., and A.G.C. conceived the research plan and designed the experiments. D.B. and T.R.O. performed the experiment, harvest plan material, and analyzed samples. T.R.O. and C.S.C. performed proteomic analysis. A.G.C. supervised the project and provide funding. D.B., S.I.Z., and A.G.C. wrote the manuscript and prepare figures. All authors read and approved the final version of the manuscript.

Data availability

RNA-Seq data files were deposited in GEO (https://www.ncbi.nlm.nih.gov/geo/) under the following accession number GSE203331. Mass spectrometry proteomic data were deposited with ProteomeXchange consortium via the PRIDE (https://www.ebi.ac.uk/pride/) partner repository with the data set identifier PXD034419.

Conflict of interest statement

None declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

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