Multiomic molecular integration in the response of cucumis sativus to biotic stress: a comprehensive analysis of the expression of protein kinases and cis-regulatory elements

Abstract

Protein kinases (PKs) play a key role in the regulation of several metabolic processes, which justifies a complete characterization of this gene superfamily. Associating its members to plant responses to biotic stresses can greatly contribute to the elucidation of the molecular basis of plant-pathogen interaction. The objectives of this study were to characterize the cucumber PK family; indicate its genomic distribution; to show expression patterns in response to biotic stimuli triggered by pathogens such as powdery mildew (PM), Alternaria leaf spot (ALS) and Root-knot Nematode (RNK), as well as to analyze the distribution of cis-elements in the potentially promoter region of differentially expressed genes. The analysis of hidden Markov models (HMMs) made it possible to classify 835 PKs in the cucumber quinoma, distributed in its seven chromosomes and categorized into 20 distinct groups and 123 families, with the RLK group being the most abundant. Evidence of tandem duplication of PK genes was also observed, enriching the understanding of the expansion of this gene superfamily in cucumber. Regarding the expression profiles in response to PM, ALS and RKN, a higher number of differentially expressed PK genes (PK DEGs) was observed in susceptible genotypes when submitted to biotrophic pathogens (PM and RKN), contrary to what was observed with the necrotrophic pathogen ALS, where a higher number of PK DEGs was found in the resistant genotype. These findings contributed to the indication of possible roles of cucumber PKs in the regulation of metabolic processes, particularly in the context of plant-pathogen interactions. It is understood that this comprehensive characterization paved the way for subsequent research into the intricate mechanisms underlying gene expression, hence cucumber's responses to important diseases. With the help of the PlantCARE platform, as well as the literature, 51,339 CREs (Cis-Regulatory Elements) were detected, which were classified into 7 major categories and 125 different types. From a further analysis, it was possible to indicate potential CREs that may be crucial for gene expression stimulated by the biotic stresses investigated in this study. Taken together, the results of this research made it possible to indicate not only candidate genes, but also CREs that can be determinant for subsequent steps aimed at the development of genotypes resistant to specific diseases.