Integrated transcriptomic and metabolomic analyses reveal key metabolic pathways in response to potassium deficiency in coconut (Cocos nucifera L.) seedlings

Front Plant Sci. 2023 Feb 13:14:1112264. doi: 10.3389/fpls.2023.1112264. eCollection 2023.

Abstract

Potassium ions (K+) are important for plant growth and crop yield. However, the effects of K+ deficiency on the biomass of coconut seedlings and the mechanism by which K+ deficiency regulates plant growth remain largely unknown. Therefore, in this study, we compared the physiological, transcriptome, and metabolite profiles of coconut seedling leaves under K+-deficient and K+-sufficient conditions using pot hydroponic experiments, RNA-sequencing, and metabolomics technologies. K+ deficiency stress significantly reduced the plant height, biomass, and soil and plant analyzer development value, as well as K content, soluble protein, crude fat, and soluble sugar contents of coconut seedlings. Under K+ deficiency, the leaf malondialdehyde content of coconut seedlings were significantly increased, whereas the proline (Pro) content was significantly reduced. Superoxide dismutase, peroxidase, and catalase activities were significantly reduced. The contents of endogenous hormones such as auxin, gibberellin, and zeatin were significantly decreased, whereas abscisic acid content was significantly increased. RNA-sequencing revealed that compared to the control, there were 1003 differentially expressed genes (DEGs) in the leaves of coconut seedlings under K+ deficiency. Gene Ontology analysis revealed that these DEGs were mainly related to "integral component of membrane," "plasma membrane," "nucleus", "transcription factor activity," "sequence-specific DNA binding," and "protein kinase activity." Kyoto Encyclopedia of Genes and Genomes pathway analysis indicated that the DEGs were mainly involved in "MAPK signaling pathway-plant," "plant hormone signal transduction," "starch and sucrose metabolism," "plant-pathogen interaction," "ABC transporters," and "glycerophospholipid metabolism." Metabolomic analysis showed that metabolites related to fatty acids, lipidol, amines, organic acids, amino acids, and flavonoids were generally down-regulated in coconut seedlings under K+ deficiency, whereas metabolites related to phenolic acids, nucleic acids, sugars, and alkaloids were mostly up-regulated. Therefore, coconut seedlings respond to K+ deficiency stress by regulating signal transduction pathways, primary and secondary metabolism, and plant-pathogen interaction. These results confirm the importance of K+ for coconut production, and provide a more in-depth understanding of the response of coconut seedlings to K+ deficiency and a basis for improving K+ utilization efficiency in coconut trees.

Keywords: Cocos nucifera L.; metabolome; physiology; potassium deficiency; transcriptome (RNA-seq).

Grants and funding

This work was supported by grants from the High-level Talents Program of Hainan Natural Science Foundation(320RC741), Hainan Natural Science Foundation Innovation Research Team Project (320CXTD444), and Hainan Key R&D Project (SQ2020XDNY0245; ZDYF2022XDNY249).